Faculdade de Ciências da Universidade de Lisboa Departamento de Geologia

(Paleo)ecology of coccolithophores in the submarine canyons of the central Portuguese continental margin: environmental, sedimentary and oceanographic implications

Catarina Alexandra Vicente Guerreiro

Doutoramento em Geologia Especialidade em Paleontologia e Estratigrafia

2013 Faculdade de Ciências da Universidade de Lisboa Departamento de Geologia

(Paleo)ecology of coccolithophores in the submarine canyons of the central Portuguese continental margin: environmental, sedimentary and oceanographic implications

Catarina Alexandra Vicente Guerreiro

Tese orientada pelo Prof. Doutor Mário Albino Pio Cachão (FCUL) e co-orientada pela Doutora Anabela Tavares Campos Oliveira (IH), especialmente elaborada para a obtenção do grau de doutor em Geologia, Especialidade em Paleontologia e Estratigrafia

2013

Faculdade de Ciências da Universidade de Lisboa Instituto Hidrográfico da Marinha Portuguesa Royal Netherlands Institute for Sea Research

Tese orientada pelo Prof. Doutor Mário Albino Pio Cachão (FCUL), co-orientada pela Doutora Anabela Tavares Campos Oliveira (IH) e pelo Doutor Hendrik Corstiaan de Stigter (NIOZ) especialmente elaborada para a obtenção do grau de doutor em Geologia, Especialidade em Paleontologia e Estratigrafia

2013

This study was performed in the framework of the European project HERMIONE (EC contract 226354) and the national project Cd Tox-CoN (FCT-PTDC/MAR/102800/2008), resulting from cooperation between the Portuguese Hydrographic Institute, Royal Netherlands Institute for Sea Research, Geology and Oceanography Centres of the University of Lisbon, Institut de Ciencies del Mar (CSIC), Barcelona, and the University of Girona. Most of the sedimentological data have been previously published by De Stigter et al. (2007, 2011), Jesus et al. (2010) and Costa et al. (2011), supported by the EU-funded projects EUROSTRATAFORM and HERMES (GOCE-CT-2005-511234), and projects “Lead in Canyons” and “Pacemaker” funded by the Netherlands Organization for Scientific Research. The candidate benefited from a PhD grant from the Portuguese Science Foundation (FCT-SFRH/BD/41330/2007).

This dissertation should be cited as: Guerreiro, C. (2013). (Paleo)ecology of coccolithophores in the submarine canyons of the central Portuguese continental margin: environmental, sedimentary and oceanographic implications. PhD Dissertation, University of Lisbon, Portugal, 251 pp. Preliminary Note

The thesis includes studies that result from collaboration with several researchers: H. de Stigter, A. Oliveira, M. Cachão, C. Sá, L. Cros, V. Pawlowsky-Glahn, C. Borges, A. Santos, L. Quaresma, J-M. Fortuño and A. Rodrigues.

According to Chapter V, article 40, paragraph 1 of the Regulation concerning Post-Graduate Studies at the University of Lisbon, which was published in the Portuguese Republic's Official Journal (Series II, no. 153, of 5 July 2003), I hereby declare that the scientific papers which have been published in (1), re-submitted (1) and submitted to (2) indexed scientific journals (one of which currently under revision), comprise the whole of this dissertation. As these studies were undertaken in collaboration with other authors, the PhD candidate hereby declares that she participated in designing and carrying out the experimental work, as well as in interpreting the results, and was responsible for drafting the manuscripts that were sent for publication.

Catarina A.V. Guerreiro

Lisbon, 3 August 2013

“To understand the part, one must understand the whole” Pickard and Emery, 1990

“No man (nor women) is an island” Adapted from John Donne (1572-1631)

À minha “família completa”, que esteve sempre lá.

Contents

Agradecimentos/Acknowledgements ………………………………………………… 11

Resumo ……………………………………………………………………………….. 13

Abstract ………………………………………………………………………………. 17

Chapter 1 General Introduction ………………………………………………….. 21 1.1 Coccolithophores …………………………………………. 23 1.2. Submarine canyons ………………………………………. 33 1.3. The Study area …………………………………………… 38 1.4. Framework and Objectives of the Thesis ………………... 44 1.5. Outline of the Thesis ……………………………………... 45 1.6. Material and Methods ……………………………………. 47

Chapter 2 Late winter coccolithophore bloom off central Portugal in response to river discharge and upwelling Continental Shelf Research (Guerreiro et al., 2013) ……...... 51

Chapter 3 Influence of the Nazaré Canyon, central Portuguese margin, on late winter coccolithophore assemblages Deep-Sea Research II, Special Issue – Submarine canyons (Guerreiro et al., re-submitted) ……………………………………………. 83

Chapter 4 Coccoliths from recent sediments of the Central Portuguese Margin: taphonomical and ecological inferences. Marine Micropaleontology (Guerreiro et al., in revision) ……...... 121

Chapter 5 Compositional Data Analysis (CoDA) as a tool to study the (paleo)ecology of coccolithophores from the central Portuguese submarine canyons. Palaeogeography, Palaeoclimatology, Palaeoecology (Guerreiro et al., submitted) ……...... 157

Chapter 6 Synthesis and Future Work …………………………………………..183

References ……………………………………………………………………………199

Appendix: A – Taxonomy of coccolithophores …………………………………. 215 B – SEM high resolution images of coccolithophores ……………… 221 C – Glossary and Abbreviations …...... 243 D – Digital Data...... 248

Agradecimentos/Acknowledgements

Fazer um doutoramento é um pouco como fazer uma maratona. É preciso muito fôlego, trabalho e persistência (nalguns casos, teimosia), à mistura com uma grande dose de curiosidade e o entusiasmo que às vezes se sente em contribuir para compreender um pouco melhor como funciona o Mundo. Para chegar sã e salva ao final da “corrida”, foi fundamental ter tido uma boa orientação, um tema de investigação entusiasmante e a colaboração e o apoio das pessoas à minha volta. E portanto, eis-me enfim, chegada ao momento de agradecer:

- to Henko de Stigter, to whom I am deeply grateful for the constant exchange of ideas, for being demanding and critical with my work, for helping me improve my writing skills, for the numerous suggestions and challenges throughout these years. You were an amazing supervisor and I have learned SO MUCH from you! Thanks to you, I am today a better researcher than I was four years ago.

- à Anabela Oliveira, por me teres apresentado o fascinante universo dos canhões submarinos, por tudo o que me ensinaste sobre a dinâmica oceanográfica e sedimentar da Margem Portuguesa e pela confiança que sempre me demonstraste desde o primeiro cruzeiro que partilhámos a bordo do NRP D. Carlos I, em 2004. Por teres sido uma amiga, para além de orientadora.

- ao Professor Mário Cachão, por ter sido o meu mentor na (paleo)ecologia de cocólitoforos, já lá vão 10 anos!, por ter incutido em mim um espírito de multidisciplinaridade, por ter ideias interessantes e por me ensinar a não ter medo de desbravar “territórios desconhecidos”.

- à Aurora Bizarro, estou grata pela amizade e confiança quase incondicional que depositou em mim desde que fui sua bolseira no projecto DEEPCO, em 2006. Por tudo o que consigo aprendi sobre a geologia da Margem Portuguesa e por, enfim, se ter deixado entusiasmar (um pouco!) pelo estudo dos cocolitóforos.

- to Lluisa Cros, moltes gràcies for everything you taught me about taxonomy and ecology of coccolithophores during my stay at Institut de Ciències del Mar (Barcelona, Spain) in 2011; also for teaching me the importance of details, and for your constant availability in discussing my data and in answering numerous questions that arose during my thesis. It was great to know you and to be able to work with you! I am also thankful to Jose-Manuel Fortuño for his friendship and technical support during the daily SEM sessions at ICM. The beautiful photographic appendix presented in this thesis was made thanks to you!

- to Vera Pawlowsky-Glahn for your permanent generosity while “translating” the basic concepts and applications of Compositional Data Analysis. It was a wonderful experience to participate in the 4th CoDA Workshop (May 2011) and to be able to work with you since then. Your constant encouragement was very important! I am also thankful to Dr. Juan Egozcue for the fruitful discussions about CoDA, and to Marc Comas for his patience while helping to unravel the “secrets” of CODAPACK.

- aos meus amigos e colegas do Instituto Hidrográfico: à Ana Santos, Maria João Balsinha, Carlos Borges, Francisco Silva, Luis Quaresma, João Vitorino, Manuela Valença, Sara Almeida e Inês Martins, pelos bons momentos partilhadas a bordo e nas reuniões dos projectos HERMES e HERMIONE, pela partilha de dados e conhecimento e por me terem ajudado, ao longo destes anos, a desvendar um pouco mais sobre os segredos do Canhão da Nazaré. Ao João Reis, Sargento Mourinho, Cassandra Pólvora e Nuno Lapa pela ajuda na colheita de amostras e pela boa camaradagem durante o cruzeiro de Março de 2010. À Catarina Fradique, Sandra Silva, Laura Reis, João Duarte, Joaquim Pombo, Luis Rosa, Aida Seabra, Fernanda Dias, Milton Cabral, Alexandra Morgado, Alexandra Caetano, Cesarina Pádua, Comandante Ventura Soares,

11 Agradecimentos/Acknowledgements

Vânia Carvalho e Nuno Zacarias, pela amizade ao longo destes anos passados no IH. Um especial obrigada à Monica Ribeiro pela cumplicidade, à Julieta Vieira pelo carinho constante e ao José Aguiar pela simpatia e pelo apoio imprescindivel na impressão da tese.

- I am very grateful to all the staff of the Marine Geology Department of the Royal Netherlands Institute for Sea Research (NIOZ), for their support, supervision, assistance and friendship during my 3 months training (2009). My special thanks go to Henko de Stigter, Wim Boer, Rineke Gieles-Witte, Thomas Richter and Henk de Haas. Also to the friends with whom I spent good times during my days living in the “Windy Island”: Catarina Leote, Raquel Santos, Vânia Freitas, Sofia Saraiva, Viola Lehmpfuhl, Joana Cardoso, Pedro Frade and Florian Ras.

- to all the crew of RV Pelagia during the BIOFUN cruise (2009) for such an amazing opportunity to learn within a multidisciplinary survey, during which some of the ideas formulated in this thesis started to mature. Also, for the great times spent at the Pelagia Pub in the end of every (laborious and yet, rewarding!) working day. A special thanks to Rachel Jeffreys, Aileen Gill, Marc Lavaleye, Elisa Baldrighi and Arie-jan Plug.

- ao Professor César Andrade, pelos bons conselhos que me foi dando pelo caminho (se não fosse por si, ainda agora estaria ao microscópio!), pela confiança, pelas boas conversas e pela amizade que já vem do tempo do trabalho da Praia de Santo Amaro (há 10 anos!); ao Carlos Marques da Silva, gostava de agradecer a enorme cumplicidade, e as generosas doses de “nervocalm” oferecidas em forma de risos e boas conversas.

- aos amigos com quem fui partilhando desabafos e risos ao longo destes anos; à Áurea Narciso, pela amizade e confiança; às futuras doutoras Alexandra Oliveira, Mónica Ribeiro e Sandra Moreira, o meu “gang” do Bairro Alto; ao Gil Machado, Rui Miranda e Rita Folha pela amizade; à Ana Margarida Bento, pela cumplicidade no NANOLAB e pelas “reservas alimentares” que me salvaram em tardes de microscópio demasiado longas; à Carolina Sá, pela divertida parceria no quarto das 4-8h a bordo do NRP Almirante Gago Coutinho e pelo fantástico trabalho de equipa que fizemos sobre o Canhão da Nazaré; ao César Jesus, meu “colega dos canhões”, pelas boas conversas que fomos tendo, sobre trabalho e não só!

- à Andreia Santos e à Fernanda André, por “cuidarem de mim” e por me ajudarem a chegar ao fim da maratona; à Aurelia Stamate pela confiança e carinho constante e pela preciosa ajuda na revisão das referências biliográficas; to Jerry, George, Elaine and Kramer for making me laugh at silly things during difficult times, and for helping me keeping my serenity (now!).

- aos meus amigos do peito, João Batalha, Nuno Batalha, Sara Ribeiro e Joana Maltez, por acreditarem em mim, por serem as pessoas que são e por estarem sempre presentes, mesmo à distância; ao “avô” José Azevedo e Silva, por me ter “empurrado” para o doutoramento e pelo apoio e confiança permanentes.

- finalmente, aos meus queridos pais, por serem o meu abrigo incondicional; às minhas irmãs e aos nossos “príncipes” Marta e Daniel pela algazarra feliz dos dias que passámos juntos; ao Fabian, pela ajuda preciosa na formatação da tese e do apêndice fotográfico, por me ter compreendido tantas e tantas vezes e por ser o meu “outro abrigo incondicional”.

- ao Instituto Hidrográfico, na pessoa do seu director, e ao Centro de Geologia da Universidade de Lisboa, pela cedência das condições de espaço e de laboratório, fundamentais à execução da do meu trabalho; um agradecimento especial ao IH pela impressão da tese; à FCT pela atribuição da bolsa de doutoramento, e aos projectos europeus EUROSTRATAFORM, HERMES, HERMIONE e Pacemaker pela colheita das amostras estudadas.

12 Resumo

A presente tese de doutoramento tem por objectivo contribuir para o conhecimento geral dos cocolitóforos na transição costeiro-neritico-oceânica, a sua distribuição ao largo de Portugal, e o seu potencial enquanto traçador (paleo)ecológico e (paleo)ceanográfico no contexto de canhões submarinos. Para compreender a relação entre os coccolitóforos e as condições ambientais, os resultados foram interpretados numa perspectiva multidisciplinar, integrados num conjunto significativo de dados relativos às características ecológicas e hidrológicas das massas de água superficiais da margem Portuguesa central (i.e. nutrientes, clorofila, temperatura, salinidade, turbidez, dados de vento e de satélite), e às caracteristicas sedimentológicas dos fundos marinhos (i.e. composição, textura e acumulação sedimentar). As variações ecológicas mais significativas observadas nas comunidades de cocólitoforos ao largo de Portugal ocorreram ao longo do gradiente costa-oceano. Dois grupos taxonómicos principais de comportamento ecológico oposto foram observados na zona fótica, marcando a transição de espécies adaptadas a regimes mais estáveis (K-selected) preferencialmente distribuídas no domínio oceânico, para espécies oportunistas (r-selected) mais frequentes nas regiões neritico-costeiras. Este gradiente também foi observado nas associações de cocólitos preservadas nos sedimentos superficiais do fundo marinho, tanto ao longo dos canhões submarinos como nas suas áreas adjacentes, embora várias diferenças tenham sido reconhecidas entre os dois tipos de ambientes. Na zona fótica, as espécies Emiliania huxleyi e Gephyrocapsa oceanica revelaram um comportamento claramente r-selected, tendo sido as principais responsáveis pelo bloom de cocolitóforos observado ao largo do Cabo Carvoeiro. Este bloom ocorreu em resposta à combinação favorável de descarga fluvial de final de inverno com ventos predominantes de norte sobre a plataforma, e condições de céu limpo. Em apenas alguns dias, as concentrações de cocolitóforos e biomassa de fitoplâncton (Chl-a) mais do que triplicaram, indicando claramente a capacidade destes organismos em tirar partido das condições favoráveis em luz e nutrientes providenciadas pela pluma fluvial superficial. As duas espécies desenvolveram-se em conjunto com outros fitoplânctónicos oportunistas (Chaetoceros s.l., Thalassiosira s.l, Skeletonema s.l.), confirmando o seu papel enquanto espécies r-selected de primeiro estádio da sucessão fitoplanctónica, caracterizadas por terem um potencial de desenvolvimento rápido em ambientes ricos em nutrientes. Coronosphaera mediterranea e Syracolithus dalmaticus também responderam positivamente às condições favoráveis no decorrer do cruzeiro, embora menos notavelmente do que as espécies anteriores. Pelo contrário, os grupos Syracosphaera spp. e Ophiaster spp. revelaram características típicas de espécies K-selected, consistentemente mais abundantes em águas mais oceânicas e menos eutróficas, afastadas da influência da pluma fluvial, ou distribuídas em níveis abaixo da pluma nas regiões mais neritico-costeiras. Gephyrocapsa ericsonii e Gephyrocapsa muellerae dominaram a comunidade de cocolitóforos sob condições de baixa produtividade na plataforma, mas não quando as águas de regiões nerítico-costeiras se tornaram favoráveis ao bloom de espécies oportunistas.

13 Resumo

No sedimento superficial de fundo, enquanto as espécies C. mediterranea, Helicosphaera carteri e a G. oceanica (e, em menor grau, Coccolithus pelagicus) registaram uma distribuição marcadamente costeira, os cocólitos produzidos pelas espécies Calcidiscus leptoporus, Umbilicosphaera sibogae, Umbellosphaera irregularis e Rhabdosphaera spp. foram observados preferencialmente distribuidos para offshore e para sul, possivelmente indicadoras de uma maior influência da ENACWst na zona mais meridional da area de estudo (i.e. a sul do Esporão da Estremadura). G. muellerae revelou ser, de longe, a espécie mais abundante e amplamente distribuída, embora geralmente mais oceânica, particularmente nas regiões adjacentes aos canhões submarinos. Enquanto certas especies mais robustas (i.e. C. leptoporus, C. pelagicus, H. carteri) tiveram um registo mais relevante no sedimento em comparação com a coluna de água, géneros de morfologia mais frágil e de menores dimensões (i.e. Syracosphaera spp., Ophiaster spp., S. dalmaticus) não foram observadas no sedimento, provavelmente traduzindo os efeitos da dissolução e fragmentação selectiva. No entanto, quando considerando percentagens de espécies de cocólitos de dimensão semelhante (≥3 µm), não foi observada qualquer evidência mais consistente de que tenha havido transporte ou preservação preferencial de especies individuais, confirmando que o signal preservado no sedimento apresenta uma forte componente (paleo)ecológica, e não meramente tafonómica. Em termos de dinâmica de canhão submarino, o Canhão da Nazaré foi observado a ter o efeito de conduta preferencial de águas oceânicas para regiões bastante proximais da plataforma continental Portuguesa, as quais se encontravam empobrecidas em nutrientes em comparação com as massas de água neríticas e costeiras durante o período de final de inverno monitorizado durante o cruzeiro. A ocorrência singular de Discosphaera tubifera e Palusphaera vandelii na cabeceira do canhão, juntamente com C. leptoporus é interpretada enquanto traçadora do deslocamento preferencial de ENACWst intensificado ao longo do troço superior do canhão, durante o inverno. Um “hotspot” de diversidade de cocolitóforos foi observado na coluna de água desta área, incluindo tanto espécies oceânicas-oligotróficas como espécies costeiras oportunistas, tendo sido interpretado enquanto reflexo da capacidade do canhão em promover trocas de massas de água entre regiões neritico-costeiras e regiões mais oceânicas, particularmente durante o inverno. Adicionalmente, a persistente ocorrência de elevadas concentrações de Chl-a à superfície obtidas por imagens de satélite, particularmente entre Março e Outubro (2006-2011), sugerem a cabeceira do Canhão da Nazaré como sendo o sector mais persistentemente produtivo do troço superior-médio do canhão. Percentagens mais elevadas de cocólitos de espécies costeiro-neriticas em sedimentos da parte superior do Canhão da Nazaré corroboram esta hipótese, possivelmente traduzindo a forte proximidade da sua cabeceira à linha de costa, resultando numa maior influência da dinâmica costeira e na sua intensificação na cabeceira e área adjacente (i.e. upwelling, ondas internas), e em condições mais dinâmicas e ricas em nutrientes para as quais as espécies r-selected estão melhor adaptadas. Pelo contrário, percentagens mais elevadas de cocólitos de espécies oceânicas no Canhão de Lisboa-Setúbal parecem traduzir um ambiente em geral mais oceânico-pelágico neste

14 Resumo canhão, resultante da sua maior distância aos efeitos da dinâmica costeira e ausência de transporte sedimentar significativo ao longo do seu talvegue, na actualidade. Uma mistura mais acentuada de cocólitos produzidos pelas duas associações (paleo)ecológicas, i.e. a costeiro-neritica e a oceânica, foi observada nos sedimentos dos canhões, em comparação com as regiões da plataforma e vertente regiões adjacentes aos canhões onde o gradiente (paleo)ecológico costa-oceano é mais distintivo. Esta assinatura nos canhões confirma a capacidade destas estrutura em promover trocas de massas de água costeiras e oceânicas (sinal ecológico), embora o importante papel das ondas internas e dos ocasionais fluxos gravíticos de sedimentos em perturbar e homogeneizar o registo sedimentar (sinal tafonómico) nos canhões deva ser sempre considerado. Ao evitar os problemas estatísticos tipicamente associados às determinações percentuais, a Análise de Dados Composicionais (i.e. a abordagem isometric log-ratio) permitiu validar e confirmar o gradiente ecológico costa-oceano observado nas associações de cocólitos no sedimento. A boa concordância entre os dois métodos sugere que o sinal (paleo)ecológico preservado na cobertura sedimentar da margem Portuguesa central é robusto, mesmo junto à costa e no contexto das condições dinâmicas vigentes nos canhões submarinos. Pelo contrário, tanto as concentrações de cocólitos (nanno/g) como os fluxos (nanno/cm2/yr) revelaram padrões de distribuição espacial onde as relações ecológicas inter- espécies parecem estar “mascaradas” por factores sedimentares/tafonómicos, particularmente nas zonas costeiras e nos canhões. O aumento de cocólitos para offshore reflecte não só a natureza primordialmente oceânica dos cocolitóforos, mas também a ocorrência de selecção textural, resultando na acumulação preferencial de cocólitos em regiões menos energéticas da vertente continental média e inferior, e em certas zonas dos canhões as quais funcionam como armadilhas morfológicas temporárias de sedimentos. Fluxos mais elevados nos troços superiores dos canhões reflectem o seu papel enquanto depocentros preferenciais de sedimentos finos na plataforma continental, tanto de origem litogénica como biogénica, incluindo cocólitos provenientes de fluxos verticais (produtividade – sinal ecológico) e laterais (resuspensão e advecção – sinal tafonómico). Este estudo ilustra cabalmente a rapidez de resposta dos cocolitóforos a variações meteorológicas e hidrográficas de curto-prazo e ao surgimento de condições ambientais favoráveis na costa Portuguesa, contrariando a noção amplamente aceite de que estes organismos representam um grupo fitoplanctónico calcário uniforme típico de ambientes de baixa turbulência, baixo conteúdo nutritivo e intensa luminosidade. Embora haja ainda muito trabalho a fazer no que respeita ao impacto dos canhões submarinos sobre a dinâmica oceanográfica e fitoplanctónica ao largo de Portugal, as associações de cocólitos preservados no sedimento revelaram-se úteis enquanto traçadores de gradientes (paleo)ecológicos e (paleo)oceanográficos vigentes na margem Portuguesa central. Os resultados confirmam estudos anteriores focados na complexa dinâmica hidro-sedimentar vigente nos canhões submarinos da Nazaré e de Lisboa-Setúbal.

15

Abstract

This thesis aims to contribute to the knowledge of coccolithophores from coastal-neritic- oceanic transitional settings, their distribution offshore central Portugal, and their potential as (paleo)ecological and (paleo)ceanographic proxy in the context of submarine canyons. In order to achieve a good understanding of the relationship of coccolithophores with the environmental setting, results were interpreted on a multidisciplinary basis, integrating a significant data set concerning the hydrological characteristics of surface waters of the central Portuguese margin (i.e. nutrients, chlorophyll, temperature, salinity, turbidity, wind data) and seabed sedimentological characteristics (i.e. sediment bulk composition, particle size and sediment accumulation). The most striking variations in phytoplankton communities off central Portugal occurred along the coastal-oceanic lateral gradient. Two principal groups of taxa of opposite ecological behaviour were observed in the photic layer, with K-selected taxa preferentially distributed in the open ocean, and r-selected taxa preferentially occurring in more coastal-neritic regions. Such gradient was also reflected in coccolith assemblages preserved in surface sediments on the seabed, both along the submarine canyons and on the adjacent shelf and slope areas, although several differences were noticed between the two environments. In the photic layer, Emiliania huxleyi and Gephyrocapsa oceanica exhibited the typical behaviour of r-selected species, being the main responsible for a coccolithophore bloom occurring in the Nazaré Canyon region (off Cape Carvoeiro). This bloom occurred in response to late winter continental runoff combined with northerly winds prevailing over the shelf, under clear sky conditions. Within a few days, coccolithophore cell densities and associated phytoplankton biomass (Chl-a) more than tripled, indicating that phytoplankton was taking profit from favourable nutrient and light conditions provided by the superficial buoyant plume. The two species were developing together with other opportunistic phytoplankton genera (Chaetoceros s.l., Thalassiosira s.l, Skeletonema s.l.), confirming their role as early succession r-selected taxa, capable of rapid growth within nutrient-rich environments. Coronosphaera mediterranea and Syracolithus dalmaticus also responded to the favourable conditions, but less so than E. huxleyi and G. oceanica. On the contrary, Syracosphaera spp. and Ophiaster spp. revealed typical characteristics of K-selected species, being consistently more abundant in more oceanic and less eutrophic waters, away from the influence of river runoff, and extending well below the nutrient-rich surface layer in the more coastal-neritic regions. Gephyrocapsa ericsonii and Gephyrocapsa muellerae dominated the coccolithophore community under steady-state low-productive conditions over the shelf, until shelf and coastal waters became favourable for r- selected species to bloom. In the seafloor sediment, coccoliths from C. mediterranea, Helicosphaera carteri and G. oceanica (and to a lesser extent, Coccolithus pelagicus) exhibited a markedly coastal distribution, whereas coccoliths from Calcidiscus leptoporus, Umbilicosphaera sibogae, Umbellosphaera irregularis and Rhabdosphaera spp. were preferentially distributed further

17 Abstract offshore and southwards, possibly tracing the preferential onflow of ENACWst into the southern part of the central Portuguese shelf (i.e. south of Estremadura spur). G. muellerae was by far the most abundant and broadly distributed species in the sediment, with highest abundances in the more oceanic areas, particularly outside the canyons. Whereas larger and more robust coccolith species (i.e. C. leptoporus, C. pelagicus, H. carteri) were better represented in the sediment in comparison to the overlying water column, smaller and more delicate species from the genera Syracosphaera spp., Ophiaster spp. and S. dalmaticus were not found in the sediments, most likely due to selective dissolution and breaking. Yet, considering the coccolith species assemblage preserved in the sediment, no consistent evidence for selective transport or preservation of individual taxa in relation to coccolith size was found, strongly suggesting the signal within the sediment is mostly (paleo)ecological rather than merely taphonomical. In terms of canyon dynamics, the Nazaré Canyon was observed to act as a preferential conduit for oceanic waters into very proximal regions of the Portuguese shelf, which were nutrient-depleted in comparison to neritic and coastal water masses during the monitored late winter period. The single occurrence of Discosphaera tubifera and Palusphaera vandelii in this proximal area, together with C. leptoporus, is interpreted as tracing the onflow of ENACWst intensified along the upper canyon during winter. A coccolithophore diversity “hotspot” was noticed in the canyon head, including both oligotrophic-oceanic and opportunistic-coastal taxa, interpreted as reflecting the canyon’s capacity to promote exchange of water masses between neritic-coastal and oceanic regions during winter. In addition, Chl-a time series obtained from satellite data (2006-2011) revealed that the canyon head is often the stage of high productivity between March and October, which makes this region the most persistently productive part of the upper-middle canyon and nearby shelf. Highest percentages of coastal-neritic coccoliths in sediments from the upper Nazaré Canyon support this hypothesis, possibly reflecting the greater proximity of the head of this canyon to the coastline. The stronger influence of coastal dynamics and their intensification in this area (i.e. upwelling, internal waves), gives rise to more dynamic and nutrient-rich conditions to which r-selected coccolithophore species are better adapted. On the contrary, higher percentages of coccoliths from oceanic taxa in the Lisbon-Setúbal Canyon suggest that a generally more oceanic-pelagic environment prevails in this canyon, explained by its greater distance from coastal dynamics and present-day lack of down-canyon sediment transport. Enhanced percentages of G. muellerae in the upper Lisbon-Setúbal Canyon may be indicating preferential onflow of oceanic water masses through the canyon and/or up- canyon transport of resuspended coccoliths in the bottom boundary layer. More pronounced mixing of coccoliths from both coastal-neritic and oceanic coccolith assemblages was observed in sediments from the canyons, in comparison to the canyons adjacent shelf-slope regions where the coast-ocean (paleo)ecological gradient is more distinctive, confirming the capacity of these structures in promoting the exchange between coastal and oceanic water masses (ecological signal). Nevertheless, the role of internal tides and occasional sediment gravity flows in disturbing and homogenizing the sedimentary record within canyons (taphonomical signal) should also be considered.

18 Abstract

While avoiding the major statistical problems potentially associated with percentages, Compositional Data Analysis involving the use of isometric log-ratios allowed validation of coast-to-ocean ecological trends determined from sediment coccolith percentages. The good agreement between the two methods suggests that the coccolith (paleo)ecological signal preserved in sediments of the central Portuguese margin is robust, even near the coast and in the context of the highly dynamic submarine canyons. On the contrary, both coccolith concentrations (nanno/g) and fluxes (nanno/cm2/yr) showed spatial trends in which ecological inter-relationships appear to be masked by sedimentary/taphonomical factors, especially towards the coast and in the submarine canyons. The general increase of coccoliths further offshore reflects the oceanic nature of coccolithophores, but also physical sorting, resulting in preferential accumulation of coccoliths within finer-grained hemipelagic sediments that accumulate in more calm environments of the middle and lower slope and in certain parts of the canyons acting as temporary sediment morphological traps. Highest coccolith fluxes in the upper canyons reflect their role as preferential depocenters of fine-grained particles both lithogenic and biogenic. Biogenic fine particles include coccoliths from vertical (productivity - ecological signal) and lateral fluxes (resuspension and advection – taphonomical signal). This study strikingly illustrates the rapid response of coccolithophores to short-term meteorological and hydrographic variability creating favourable conditions for growth off central Portugal. These results contradict the accepted notion of coccolithophores being a uniform functional group of calcifying phytoplankton thriving in low-turbulence, low-nutrients and high-light environments. Whereas much work still needs to be done concerning the impact of the canyons on both oceanography and phytoplankton dynamics off central Portugal, coccoliths preserved in the seabed sediment appeared to be useful tracers of the prevailing (paleo)ecological and (paleo)oceanographic trends. The results support previous studies focused on the complex hydro-sedimentary dynamics prevailing in the Nazaré and Lisbon-Setúbal canyons.

19

Chapter 1

General Introduction

Chapter 1

General Introduction

1.1. Coccolithophores

Coccolithophores are marine, unicellular phytoplankton organisms, belonging to the Kingdom Chromista, phylum Haptophyta and division Prymnesiophyceae. They represent the main component of extant calcareous nannoplankton (Jordan and Chamberlain, 1997; Jordan et al., 2004). Coccolithophores are one of the main groups of marine phytoplankton, distinguishable from other groups by the presence of a calcified exoskeleton at some stage in their life cycle, composed of numerous minute calcified scales (1-16 µm across), the coccoliths. These coccoliths, produced by biomineralization of minuscule calcite crystals arranged according to characteristic arrays, exhibit morphological and optical patterns that have taxonomic and phylogenetic meaning (Pienaar, 1994; Young, 1994). Coccolithophores are among the most important pelagic calcifying organisms in the moderns oceans (Baumann et al., 2004; Hay, 2004). Their coccoliths abound in seafloor sediments and present one of the most abundant and continuous fossil records since the Late Triassic to the present day (e.g. Bown et al., 2004). Coccoliths preserved in the geological archive store valuable information on (palaeo)environmental conditions from the photic zone (McIntyre and Bé, 1967; Roth, 1994; Baumann et al., 2000; Boeckel and Baumann, 2008) and thus can be used as indicators of paleoceanographic processes, sea surface water masses, productivity and climate change (e.g. Beaufort et al., 2001; 2011; Flores et al., 2000; Ziveri et al., 2004; Silva et al., 2008). It is estimated that about 20–60 % in weight of marine pelagic carbonate is produced by coccolithophores (Brand, 1994; Winter et al., 1994). Coccoliths are, by far, the most common (sub)fossil structure than can be found in a simple smear of ocean sediment, particularly in oozes. Therefore, coccolithophores are not only important in the marine ecosystem as primary producers, but also as contributors of inorganic carbon to the marine carbonate pump (Bown, 1998; Rost and Riebesell, 2004). In addition, they are likely to produce additional feedback on global climate due to enhanced albedo resulting from the highly reflective masses of detached coccoliths and production of dimethylsulphonium propionate – DMSP, thought to play a role in reducing solar irradiation (Westbroek et al., 1993; Malin and Steinke, 2004).

23 Chapter 1

Morphology and Biology

The taxonomy of coccolithophores is based on the morphology and optical properties of the coccoliths covering the cell. The crystallographic features of calcite are used to identify different coccolithophore species, i.e. the birefringence and extinction patterns of calcite crystals when viewed in cross-polarized light, which are distinct for different coccolithophore genera according to the specific crystallographic arrangement of their coccoliths (e.g. Young and Bown, 1991). There are two major groups of coccoliths: the holococcoliths, composed of numerous minute euhedral calcite crystals, whose biomineralization is supposed to occur outside the cell; and the heterococcoliths, which are the most common forms in the sediment, composed of radially continuous series of variably shaped crystal units biomineralized intracellularly (see Piennar, 1994; Young et al., 1997; Young and Henrikson, 2003). Within these basic groups, a high morphological diversity is observed. Among the heterococcoliths, the most important morphological categories are: placoliths (e.g. Emiliania huxelyi, Gephyrocapsa spp., Coccolithus pelagicus s.l., Calcidiscus leptoporus, Umbilicosphaera sibogae), helicoliths (e.g. Helicosphaera carteri), caneoliths (e.g. Syracosphaera spp., Ophiaster spp., Coronosphaera mediterranea) and rhabdoliths (Rhabdosphaera spp., Discosphaera tubifera) (see Young et al., 1997; Cros, 2000) (Figure 1.1).

Figure 1.1 - Examples of different types of coccospheres and coccoliths (http://www.geo.uni-bremen.de). The term “nannoliths” refers to nannofossils which are thought to be related to coccolithophores, but exhibiting structures that are neither heterococcoliths nor holococcoliths (e.g. Braarudosphaera bigelowi).

24 General Introduction

Coccolithophore cells may have coccoliths that are all of the same size and morphology, but they may also have different coccolith forms (i.e. dimorphism and polymorphism e.g. Syracosphaera spp.) and sizes. Most coccolithophores have different types of coccoliths for distinct life-stages (e.g. C. pelagicus s.l.) (see Piennar, 1994). In most cases, coccoliths are arranged in a single layer outside the body organic scales, whereas some taxa may exhibit two distinct layers of heterococcoliths of different types (i.e. dithecatism) (Cros, 2000). Others produce multi-layered coccospheres composed of numerous uniform coccoliths (e.g. E. huxleyi) (see Billard and Inouye, 2004). Various explanations have been given for the function of coccoliths: protection of the cell membrane, protection from predation, cellular buffering, ballast for increasing sinking rate, aiding nutrient absorption in turbulent environments (e.g. placolith-bearing taxa), enhancing surface area to decrease sinking in low turbulence environments (e.g. spines and spiral coccoliths), light focusing aiding photosynthesis in low-light environments (see Young, 1994). The high morphological diversity of coccoliths and coccospheres may also reflect distinctive ecological strategies preferred by different coccolithophore taxa; e.g. placolith-bearing taxa are more associated to eutrophic environments, such as upwelling areas and shelf-seas, where light and nutrient levels are favourable for rapid population growth (r-selected), whereas “umbelliform” taxa are more often associated to low-latitude oligotrophic environments (K- selected) (see Young, 1994) (Figure 1.2) .

Figure 1.2 –Ecological distribution of coccolithophore types representing a transect from continental shelf to mid-ocean at low latitudes. Arrows represent nutrient supply driven from river runoff and coastal upwelling between the continental shelf and slope. Dashed lines are delimiting the lower photic zone (adapted from Young, 1994).

The life cycle of coccolithophores is heteromorphic, with alternating haploid (mobile and flagellate) and diploid generations (non-mobile, without flagellates), produced by mitotic division and syngamy, respectively (Figure 1.3). Typically, diploid cells produce heterococcoliths, whereas haploid cells produce holococcoliths (see Billard and Inouye, 2004; Houdan et al., 2003). “Combination coccospheres” composed of both types of coccoliths are interpreted as cells that were captured right after a life-cycle transition (Cros et al., 2000; Geisen et al, 2002; Frada et al., 2009). Whereas little is known yet about the factors that trigger phase

25 Chapter 1 changes in coccolithophores, it has been proposed that phase changes represent an evolutionary mechanism for genetic recombination in marine planktonic organisms that are forced to deal with constantly changing environmental conditions (Baumann et al., 2005). Other authors have proposed that their ability to grow under two phases may have a primary ecological significance, either as strategy for a species to exploit a wider range of environmental conditions (e.g. Cros et al., 2000), and/or to rapidly escape negative selection pressures carried on one stage, such as grazing, parasitic attack or viral infections (Frada et al., 2008), or abrupt environmental changes (Noel et al., 2004). Reproduction rates observed in the laboratory were highest for Emiliania huxleyi (up to 2.7 divisions per day), followed by Gephyrocapsa oceanica and Calcidiscus leptoporus (1.2 div. per day) (Brand, 1982). Field observations by Cachão and Moita (2000) indicated a growth rate of 1.4 divisions per day for Coccolithus pelagicus during a moderate upwelling event offshore Portugal.

Figure 1.3 – Schematic illustration of coccolithophorid life cycles. Diploid and haploid phases produce heterococcoliths and holococcoliths, respectively, here illustrated by scanning electron microscope images of Calcidiscus leptoporus (left) and Calcidiscus quadriperforatus (right), respectively. The combination coccosphere shown in the middle, which has both types of coccoliths, represents a transition from haploid to diploid phase (from Young and Henriksen, 2003).

26 General Introduction

Ecology and Biogeography

Coccolithophores, like all other photosynthesizing plankton groups, are restricted to the photic zone of the oceans. Within this upper ocean layer, turbulence is important in controlling access of phytoplankton to light and nutrient. According to the “Margalef Mandala”, which classifies phytoplankton groups in terms of their response to nutrients vs. turbulence following a mixing event, coccolithophores occupy an intermediate position between diatoms, – fast- growing r-selected organisms adapted to profit from nutrient availability in eutrophic and turbulent environments -, and dinoflagellates – slower-growing K-selected organisms adapted to stratified, low-nutrient environments ( Margalef, 1978) (Figure 1.4). However, the “Margalef Mandala” was mostly based on the ecological behavior of E. huxleyi, which is nowadays known to be a somewhat atypical coccolithophore, often acting as an early succession r-selected species and reported to produce extensive blooms in various regions of the ocean (e.g. Winter et al., 1994; Tyrell and Merico, 2004; Souza et al., 2011). As a group, the coccolithophores are considered to be K-selected, as they reach their highest diversity and relative abundance within the phytoplankton community in warm, stratified oligotrophic waters from low and middle latitude regions, as opposed to eutrophic environments such as coastal-neritic waters, where they are less diverse and surpassed in abundance by diatoms (e.g. McIntyre and Bé, 1967; Winter et al., 1994; Brand, 1994; Ziveri et al., 2004). Nevertheless, several taxa reveal a clear r-selected behaviour, e.g. placolith-bearing taxa such as E. huxleyi and G. oceanica, as indicated by their occurrence in blooms in the oceans (e.g. Knappertsbusch and Brummer, 1995; Souza et al., 2011) (Figure 1.5), and within turbulent coastal and mature upwelled waters (e.g. Ziveri et al., 1995; Baumann et al., 2000; Cachão and Moita, 2000; Moita, 2001; Moita et al., 2010; Silva et al., 2008). Overall, coccolithophore species appear to be distributed along nutrient gradients from the eutrophic coastal and polar regions to oligotrophic central gyres, thus reflecting r- and K-selection biological characteristics respectively (Brand, 1994).

Figure 1.4 –Margalef’s Mandala (Margalef, 1978) re-drawn by Balch (2004)

27 Chapter 1

The general biogeography and habitat characteristics of coccolithophores are known from plankton and seafloor sediment surveys (McIntyre and Bé, 1967; Brand, 1994; Roth, 1994; Winter et al., 1994; Young, 1994; Ziveri et al., 2004). Temperature controls the largest-oceanic scale distribution following broad latitudinally defined biogeographical zones related with the major oceanic water masses (McIntyre and Bé, 1967; Winter et al., 1994). Five major floral zones have previously been defined by McIntyre and Bé (1967): Subarctic/antarctic, Temperate, Subtropical and Tropical. This broad-scale zonation, however, does not take into account local phenomena such as coastal currents, gyres, eddies, upwelling, river runoff, which regionally affect their distribution (Cachão and Moita, 2000; Andruleit et al., 2003; Ziveri et al., 2004; Andruleit, 2007; Silva et al., 2008; Guerreiro et al., 2013 – see Chapter 2). Changes in temperature will most likely affect sub-polar and temperate populations whose ecology is dependent on the seasonal thermocline, as opposed to species from subtropical regions where a permanent thermocline is present: whereas coccolithophore species are present in the tropics during the entire year, in temperate regions, they are only abundant in spring- summer (e.g. Brand, 1994; Andruleit et al., 2003). Whereas most coccolithophore species preferentially dwell in the upper 50–80m of the photic layer, most species appear photo- inhibited very close to the surface. E. huxleyi, however, stands out for its tolerance to high light levels, possibly contributing to its capacity to dominate coccolithophore assemblages (Tyrell and Merico, 2004). Other species of coccolithophores live almost exclusively between 100 and 200 m, in the lower photic zone (e.g. Florisphaera profunda, see Brand, 1994).

Figure 1.5 - Satellite image of an Emilinia huxleyi bloom in the English Channel off the coast of Cornwall, 24 July 1999 (http://www.noc.soton.ac.uk/soes/staff/tt/eh/satbloompics.html).

28 General Introduction

Vertical Transport and Sedimentation

Coccoliths provide a particularly useful calibration link with ecological and oceanographic conditions since they reflect the hydrological patterns persistent or strong enough to be preserved in the fossil record as revealed by several studies. Indeed, although subjected to a variety of post-mortem (biostratonomical) processes after death of the coccolithophore cell, studies indicate that coccolith thanatocoenosis in surface sediments can be closely related to the coccolithophore communities dwelling in the overlying photic layer (e.g. Abrantes and Moita, 1999; Baumann et al., 2000; 2005; Kinkel et al., 2000; Sprengel et al., 2002; Boeckel and Bauman, 2008). Such is the particular case of heavier calcified and resistant forms (C. leptoporus, C. pelagicus, H. carteri), which have higher preservation potential, and high cell densities species (E. huxleyi, Gephyrocapsa spp.) which are more abundant due to seasonal high productivity (e.g. Baumann et al., 2000; Ziveri et al., 2004; Baumann et al., 2005; Boeckel and Baumann, 2008). This good correspondence, as well as the good preservation of coccoliths even in sediments below the calcite compensation depth, can be attributed to their rapid transfer from the photic zone to the sediment through incorporation in fast-sinking faecal pellets produced by grazing zooplankton and within marine snow aggregates (Roth, 1994; Steinmetz, 1994; Balch, 2004). Otherwise, taking the very slow settling of individual coccoliths into account, being on the order of a few cm per day, it would take a single coccolith on the order of a century to reach the bottom of the ocean, making it very unlikely that it would escape from dissolution and displacement by currents far beyond the production area (see Steinmetz, 1994). Faecal pellets, in addition to providing rapid transport of intact coccospheres and individual coccoliths at average sinking rates of 200 m/day, they also provide protection to coccoliths by enclosing them in an organic membrane that acts as a chemical barrier. Whereas one single pellet may carry 100,000 coccoliths, the mismatch between coccoliths and coccospheres in sediment traps seems to be 3-4 order of magnitude (e.g. Broerse et al., 2000; Ziveri et al., 2000ab). This happens because the latter are fragile and easily disintegrate after organic membranes holding the coccoliths together have been digested by herbivorous zooplankton or metabolized by bacteria during transport to the seafloor, while lying on the seafloor, or after burial (Roth, 1994). Because of the importance of faecal pellets in the vertical transport of coccoliths, coccolith-rich sediments are more commonly found below mixed, productive surface waters where coccoliths may not be the dominant phytoplankton group but where grazing is important, rather than below oligotrophic waters where coccolithophores are dominant but where grazers are less abundant (Balch, 2004). Despite the efficiency of faecal pellets in protecting coccoliths and accelerating their vertical transport, the correspondence between living coccolithophore communities and coccolith assemblages preserved in the seabed is still complex. In the first place because the seabed sediment contains a time-integrated collection of the seasonally variable flux of coccoliths arriving from the ocean surface layer. Subsequent bioturbation of the uppermost few centimetres of sediment will easily mix coccoliths produced over a timespan of hundreds of years. On top of that, resuspension of surface sediments by bottom currents may result in sorting

29 Chapter 1 and selective destruction of coccoliths, whilst coccoliths from allochtonous production or reworked from older deposits may be introduced. The result will be a more or less homogenised coccolith taphocoenosis. The gradual loss of primary ecological information occurring from the initial production of coccolithophores in the photic layer until the final incorporation of coccoliths in the sedimentary record was well illustrated by studies performed in the Arabian Sea, where coccolithophore species composition in water samples, sediment trap samples and surface sediments were compared (Andruleit et al., 2003; Andruleit and Rogalla, 2002; Baumann et al., 2005). The study demonstrated that the great variability in plankton samples was not preserved in the annual cycle from the sediment traps, whereas the annual mean composition from the traps closely resembled the sedimentary record, which represented a mixed signal of intra-annual species succession. According to these authors, the good correspondence of species composition and relative abundance between the annual mean of sediment trap samples and surface sediments suggests that the information record from the traps is likely to be transformed into the sediment almost without biases in the species relative abundances (Baumann et al., 2005).

Coccoliths as (paleo)ecological proxies in coastal regions

Whereas coccolithophores are generally studied in the oceanic domain where the highest concentrations and diversity occur, several studies demonstrated the ability of this group to profit from the high nutrient conditions driven by coastal upwelling and river runoff (e.g. Cachão and Moita, 2000; Silva et al., 2008; Guerreiro et al., 2013 – Chapter 2). However, the relationship between living communities and coccolith species assemblages preserved in the seabed may be particularly complex within shallower marine environments such as continental shelves (e.g. Steinmetz, 1994; Roth, 1994). Dilution by terrigenous material and dissolution caused by oxidation of organic matter in sediments are additional factors that affect the concentration and composition of coccolith assemblages in sediments from shallow marginal seas (Roth, 1994). In addition, the increasing bottom water hydrodynamics towards the coast will expectedly have a major control on coccolith accumulation in the sediment; whereas winnowing by waves and currents hampers the accumulation of coccoliths in coarse-grained deposits of the shelf and upper slope, coccoliths will preferentially accumulate in fine-grained hemipelagic deposits that accumulate in more quiescent environments of the middle and lower slope (see Chapter 4). Reworking of sub-fossil or fossil specimens by strong bottom currents in continental shelf and slope regions may also be a problem when making ecological inferences from sediment coccolith assemblages (e.g. Ferreira et al., 2008). Complexity further increases in heterogeneous and dynamic regions such as submarine canyons, where the factors above are known to be intensified (i.e. intensified coastal dynamics; bottom resuspension by internal tides and gravity flows; De Stigter et al., 2007; 2011). A deep knowledge of the oceanographic and sedimentary processes prevailing in these areas is essential to study coccolith sedimentation in marginal-marine settings, for which a

30 General Introduction close cooperation between nannoplankton specialists and physical, chemical and biological oceanographers, and marine sedimentologists is required.

Coccolithophores off central Portugal

The first study on the coccolithophores off Portugal was based on the coccoliths sedimentary record from shelf-to-slope transects in the Portuguese margin, performed by Cachão (1993), revealing a general increase of coccolith species diversity further south. Highlights from this study refer to the tendency of Calcidiscus leptoporus and Rhabdosphaera spp. to decrease their relative abundance towards the coast, whereas Gephyrocapsa spp. was more generally abundant in neritic-coastal regions, and Helicosphaera carteri was more abundant north of the Nazaré Canyon. The increase of H. carteri further north was later supported by both sediment and water column studies: an extremely high percentage of this species (~85 %) was found in sediments from the mouth of the Douro river by Guerreiro et al. (2005), interpreted as reflecting an opportunistic behaviour possibly related with locally confined nutrient-rich conditions, whereas Moita et al. (2010) observed H. carteri being more abundant in the photic layer west of this river, during winter. Abrantes and Moita (1999) and Moita (2001) were the first to study the annual (summer- fall of 1985 to winter-spring of 1986) composition and seasonal spatial variation of phytoplankton in the Portuguese continental margin. According to these authors, diatoms were the major phytoplankton group during upwelling conditions, whereas coccolithophores were dominant (>90 %) during winter, associated with warmer and nutrient-depleted subtropical waters flowing onto the Portuguese shelf. Living coccolithophores revealed a broad distribution, but more abundant south of the Nazaré Canyon in both summer and winter sampling periods. North of Nazaré, this group occurred mainly on the mid- and outer-shelf. The sediment record reflected not only the general north-south difference observed in the water column for both upwelling and non-upwelling situations, but also the summer water distribution (Abrantes and Moita, 1999). According to these authors, the sediment distribution pattern preserved most of the original biological spatial variability independent of the sediment lithology and/or sedimentary processes acting on the Portuguese shelf, particularly concerning the record of coccolithophores produced during blooms. More detailed analysis of the coccolithophores communities thriving off Portugal during winter was later performed by Cachão et al. (2000). The entrainment of subtropical water masses, originating from south of the Azores Front into the Iberian Poleward Current during this period, was reflected in coccolithophore assemblages by the occurrence of subtropical species like Algirosphaera quadricornu, Alveosphaera bimurata, Cyclolithus annulus, Florisphaera profunda, Michaelsarsia elegans, Syracosphaeara lamina and Turrilithus latericioides, along with temperate species like Gephyrocapsa muellerae, Gephyrocapsa ericsonii and Emiliania huxleyi.

31 Chapter 1

Cachão and Moita (2000) brought new insights on the ecological preferences of C. pelagicus, a formerly considered typical sub-arctic coccolithophore species. These authors observed living C. pelagicus consistently associated to riverine plumes and shelf-break fronts off Portugal, and an increase of its coccolith abundances in surface sediment assemblages off Douro, Ave and Cávado rivers (NW Portugal). This was interpreted as reflecting a relation between C. pelagicus and moderate turbulence conditions combined with nutrient availability, proposing this species as a tracer of the periphery of areas of enhanced productivity. Morphometric analysis later performed by Parente et al. (2004) revealed the existence of three morphotypes of C. pelagicus (s.l.), each revealing specific ecological features: the smaller-sized, related to C. pelagicus subsp. pelagicus, interpreted as a proxy of the influence of subpolar Atlantic water masses west of Portugal; the intermediate-size, related to C. pelagicus subsp. braarudii, possibly related to coastal upwelling; and the larger, described as C. pelagicus subsp. azorinus, which seemed to indicate the influence of water masses driven directly from the Azores front. More recently, during a four years weekly survey, Silva et al. (2008) performed the first systematic investigation of the coccolitophore assemblages from offshore Portugal. This study confirmed the general preference of the group for non-upwelling conditions, although certain species appeared capable of withstanding coastal turbulence and well-adapted to the nutrient- rich coastal environment. A recurrent and distinct seasonal succession and interannual differences were observed, related with intensity and length of upwelling-downwelling seasons (and related temperature variations) and precipitation (and related salinity variations). According to these authors, Emiliania huxleyi and Gephyrocapsa spp. revealed to be good proxies for coastal surface productivity waters as they responded quickly to a decrease in turbulence during upwelling events, in particular during spring and summer; G. muellerae and G. ericsonii were more abundant in colder waters associated with the beginning of the upwelling season, whereas Gephyrocapsa oceanica was more productive during summer; C. pelagicus was also related to upwelling, possibly responding to shifts in the position of the Cape Roca filament relatively to Cascais position; Coronospheara mediterranea, Syracosphaera pulchra, H. carteri and Rhabdosphaera clavigera revealed to be tracers of the onflow of subtropical warmer and saltier waters over the shelf during the transition from upwelling to downwelling season (e.g. Moita et al., 2010); finally, the oceanic preference of C. leptoporus was confirmed, revealing to be a good tracer for the convergence of oceanic waters during winter. In the Nazaré Canyon area, a general characterization of the calcareous nannoplankton assemblages preserved in surface sediment samples carried out by Guerreiro et al. (2009) suggested that the canyon’s hydro-sedimentary dynamic regime may prevent the deposition and/or preservation of the smaller and fragile species (e.g. E. huxleyi and G. ericsonii), while enhancing the record of the larger ones (e.g. G. oceanica). Evidences of local enhanced productivity are reported from near the canyon possibly related to persistent physical phenomena resultant from the canyon’s morphology and proximity to the coast (e.g. solitary internal waves; Quaresma et al., 2007), and/or upwelling enhancement in the canyon head .

32 General Introduction

These hypotheses were later corroborated by a phytoplankton pigments study performed by Mendes et al. (2011) in this region; maximum values of 19’ hexanoyloxyfucoxantine, the pigment used as a proxy for the coccolithophores, were found north of the canyon, and the maximum values of chlorophyll-a were recorded in the inner shelf north of the canyon’s head where the highest coccolith abundances were found.

1.2. Submarine canyons

Submarine canyons are prominent topographic features dissecting the seafloor of most of the world’s continental margins, cutting through all substrates, from unlithified sediment to crystalline rock. Canyons typically start off on the shelf and upper slope as deeply incised valleys generally with a V-shaped profile and with deep and steep, gullied slopes, gradually changing to shallower valleys with U-shaped profile as depth increases. At the base of the continental slope a great decrease in the canyon wall height occurs, and often the canyon passes into deep-sea channels bordered by natural levees (e.g. Shepard, 1964). Whereas some canyons cut across the shelf all the way to the coast, others may just indent the outer shelf. Coastal canyons typically exhibit sizes comparable to those of Grand Canyon, i.e. width of ~10-30 km and depth ~2 km (Hickey, 1995) (see Figure 1.6). The formation of submarine canyons results from a dynamic interplay of erosional and depositional processes controlled by tectonics, terrestrial sediment input, and regional oceanography (Shepard, 1981; Hickey, 1995; Lastras et al., 2009; Masson et al., 2011). Whereas canyons are nowadays thought to evolve from localized small furrows on the upper slope along which slope instability and sediment failure in the form of gravity-driven flows eventually leads to their retrogressive development and enlargement (Pratson and Coakley, 1996; Arzola, 2008; Lastras et al., 2009), a limited number of fundamental processes acting in different geological and geographic, climatological and oceanographic settings is likely to result on a wide range of different canyon morphologies. Geomorphological and sedimentary observations reveal that much of their present-day morphology resulted from enhanced sediment transport during periods of sea-level low stands, when the continental shelves were exposed and presented a better connectivity between fluvial systems and canyon heads (Normark and Piper, 1991). During sea-level high stands, submergence of the shelf drastically reduced the role of canyons as preferential pathways of coarse sediment towards to the deep-sea, resulting in predominant hemipelagic sedimentation (e.g. Weaver and Kuijpers, 1983; Canals et al., 2006; Palanques et al., 2008; Martin et al., 2011; Li et al., 2012), with much of the fine-grained and organic material transported being nowadays retained in the canyons’ upper and middle sections (Van Weering et al., 2002; De Stigter et al., 2007; 2011). Nevertheless, those canyons that are deeply incised into the continental shelf still preserve a certain degree of activity, as they continue to receive and transport fine-grained sediments supplied by coastal and shelf currents. Extreme river floods, strong storm events, dense water cascading and earthquakes are considered the most important triggers for the occurrence of

33 Chapter 1 episodic canyon-flushing events, able to carry sediments from the shelf down to the abyssal plain (e.g. Palanques et al., 2005; Canals et al., 2006; Palanques et al., 2005; De Stigter et al., 2007; 2011; Martin et al., 2011; Masson et al., 2011). Closely related to their impressive morphology, submarine canyons are complex, heterogeneous and highly dynamic marine environments. While linking the land intimately with the deep ocean, canyons may act both as (1) temporary depositories of sediment particles and organic matter in transit along the coast and shelf, (2) preferential conduits through which the

Figure 1.6 – Scheme of a submarine canyon dissecting the continental shelf and slope (above) (Encyclopedia Britannica, Inc., 2006); bathymetric high-resolution maps of Monterey Canyon (off California, on the left) (http://www.mbari.org) and Nazaré Canyon (off Portugal, on the right) (data from Portuguese Hydrographic Institute). transport of particles between the coastal domain and the deep-sea is intensified (e.g. dense- water cascading and gravity-driven flow events; Schmidt et al., 2001; Van Weering et al., 2002; Oliveira et al., 2007; Canals et al., 2006; De Stigter et al., 2007; 2011), and (3) modifiers of coastal circulation, interrupting the along-slope geostrophic flow and thus leading to enhanced shelf-slope exchange of water and organic/inorganic matter (e.g. Hickey et al., 1986; Durrieu de Madron, 1994; Monaco et al., 1999; Puig et al., 2003). Canyons affecting water mass flow and sediment exchange between shallower and deeper regions have a strong impact on both pelagic and deep-sea benthic biological communities, often reflected in enhanced productivity and

34 General Introduction species diversity (e.g. Hickey, 1995; Ryan et al., 2005; Tyler et al., 2009; Cunha et al., 2011; Contreras-Rosales et al., 2012; Morris et al., in press). Measurements in submarine canyons are among the most difficult in the ocean mostly due to their complex and heterogeneous topography and the extremely steep walls, and the presence of strong bottom currents (e.g. Hickey, 1997; Masson and Tyler, 2011). The introduction of new geophysical techniques has been crucial to allow more detailed geomorphological and bottom sedimentary descriptions of these systems, making the canyons more accessible to safely obtain sediments samples, CTD profiles and to deploy moored instruments.

Impact on regional oceanography

Submarine canyons are areas of increased exchange between oceanic and coastal water masses, exhibiting intensified flow and turbulence in comparison to the adjacent shelf and slope, potentially affecting coccolithophore communities in their vicinity. Both observations and numerical models demonstrate that canyons modify regional current patterns, changing magnitude and direction of currents. Pressure-driven, wind-driven and tidal flows dominate water motion within canyons (Hickey, 1995; Klinck, 1996; Allen and Durrieu de Madron, 2009). Whereas shelf and slope currents usually follow the isobaths due to geostrophic constraints, once they are intersected by canyons, a new dynamic balance that is not geostrophic is produced; the along-flow will be focused by the canyon topography until it crosses the isobaths, resulting in enhanced cross-slope and cross-shelf exchange along the canyons. This cross-isobath flow tends to enhance wind-driven upwelling and downwelling currents, and cascading flows of dense water into the ocean. In addition, vertical water movements associated to wind-driven currents and internal tidal activity will be locally enhanced in the canyons and adjacent areas, due to topographic funneling of water (Hickey, 1997; Allen and Durrieu de Madron, 2009). Narrow canyons have a relatively strong effect on the oceanographic circulation, whereas wider canyons mainly distort the flow to occur along isobaths. Near the sea surface, the flow passes unhindered across the canyon, but closer to the canyon rim, the flow is redirected along the canyon axis with the occurrence of upwelling or downwelling occurrin depending on the direction of the winds (Klinck, 1996; Hickey, 1997; She and Klinck, 2000; Palanques et al., 2005). The mean flow within a few hundred meters of the canyon floor is predominantly directed up- or down-canyon, constituting a very important mechanism for resuspension and transport of sediments from the shelf and slope to the deep-sea. Stratification of the water column reduces the canyon’s topographic effect on the coastal flow (Klinck, 1996; She and Klinck, 2000 and references therein). Under upwelling-favorable wind conditions in Eastern Boundary Systems like the Portuguese continental margin, downwelling of shelf water occurs along the northern canyon

35 Chapter 1 rim (upstream side) whereas upwelling occurs along the canyon axis and southern rim (downstream side) (Allen, 1996; Hickey, 1997, Klinck, 1996). Large volumes of water are pumped out of a canyon during upwelling events, which may result in an onshore flow up to 50 times more than occurring over the adjacent shelf and slope (Allen, 1996). During strong wind events, intensification of upwelling in canyons may result in vertical velocities of up to 80 m/day (Hickey, 1997), bringing nutrient-rich water from depths up to 300 m to the canyon rim and onto the adjacent shelf (She and Klinck, 2000). The up-canyon deflection of deeper offshore currents can induce a strong nutrient transport into the euphotic zone, in the continental shelf, stimulating primary production on the shelf and nearshore areas (in Skliris and Djenidi, 2006). Under downwelling-favorable wind events, the circulation generated within the canyon is largely opposite to that forced by upwelling winds, creating strong flow toward the shelf and coast resulting in downwelling (Klinck, 1996; She and Klinck, 2000). A 3-D numerical modeling study performed for the Calvi Canyon (NW Corsican coast) showed that convergence under downwelling-favorable winds is amplified along the canyon, such that the canyon is acting as a trap of shelf water (Skliris and Djenidi, 2006). In addition to pressure-driven and wind-driven circulation, tidal flows that usually run parallel to the shelf-break topography will be intersected by the presence of a narrow submarine canyon, resulting in regions of intensified and focused baroclinic tides and internal waves, leading to strong vertical mixing within and around the canyon (e.g. Hickey, 1995; Allen and Durrieu de Madron, 2009; De Stigter et al., 2007). This process may result in higher particulate and nutrient concentrations in the water column within the canyon (e.g. Bosley et al., 2004; Ryan et al., 2005). Where canyons cut across the entire width of a continental shelf, the interaction between tidal currents and the canyon rim may result in internal waves that propagate from the canyon across the adjacent shelf, increasing bottom turbulence and thereby favouring bottom sediment resuspension and transport (Huthnance et al., 2002; Quaresma et al., 2007).

Impact on marine ecosystems

Whereas the majority of studies on submarine canyon ecology are focused on the benthic system, exhibiting enhanced productivity associated with the accumulation of labile organic matter, a strong response from plankton in the vicinity of canyons has also been reported from both in situ observations (e.g. Allen et al., 2001; Bosley et al., 2004; Palanques et al., 2005; Ryan et al., 2005; 2010) and numerical models (Skliris and Djenidi, 2006). This is partially explained by the enhancement of upwelling at and near the canyons, providing a nutrient source that increases phytoplankton and zooplankton productivity (Hickey, 1995; Allen, 1996; Klinck, 1996). Funneling and trapping of plankton (e.g. Macquart-Moulin and Patriti, 1996; Skliris and Djenidi, 2006)) and resuspension phenomena driven by increased bottom turbulence in canyons (e.g. Bosley et al., 2004; Ryan et al., 2005) are additional factors leading to enhanced

36 General Introduction productivity in these regions. Recirculation within canyons also favors a prolonged residence time of nutrients and biota in these areas (Hickey, 1995; 1997; Allen et al., 2001). There is strong evidence to suggest that submarine canyons have an important effect on the entire marine food chain, from phytoplankton to marine mammals. Some examples are given below: A three-dimensional hydrodynamic model used to investigate plankton dynamics in the Calvi Canyon (NW Corsica) showed maximum concentrations of phytoplankton occurring over the canyon and downstream of the canyon mouth, and trapping of phytoplankton biomass by the cyclonic circulation within the canyon (Skliris and Djenidi, 2006); In the vicinity of Astoria Canyon (west coast of North America), local primary production may have a dominant role on the canyon food web in comparison to other potential sources. Densities and biomasses of some micronekton species were higher in the canyon in comparison to nearby areas, suggesting that the distribution of these organisms was affected by currents modified by the canyon topography (Bosley et al., 2004); In the Palamós Canyon (NW Mediterranean) chlorophyll concentrations were found to be higher in its upper section (from the canyon head to about 1200 m) in comparison to its lower section (deeper than 1200 m), suggesting a direct biological input from the coastal productivity into the canyon system. Extremely high concentrations of cysts of a variety of planktonic organisms, including dinoflagellates, tintinnids and calanoida, were found in sediment traps from the Foix Canyon and Palamós Canyon, in comparison to much lower concentrations from the slope adjacent to the canyon, suggesting preferential accumulation driven by the hydrodynamics prevailing in the canyons and neighboring areas (Della Tommasa et al., 2000; Palanques et al., 2005). Alvarez et al. (1996) reported high fish larval density on the rims of Palamós canyon, much larger than in the shelf area, whereas Macquart-Moulin and Patriti (1996) found accumulations of migratory micronekton crustaceans over submarine canyons on the NW Mediterranean. David and Di-Méglio (2012) reported that these canyons are preferential sites for gathering of marine mammals, apparently related to food availability; In the Barkley Canyon (SW off Canada), superficial zooplankton species were found to be carried across the canyon with little deflection from their normal cross-shelf position, whereas the deeper species were observed to be displaced in shoreward direction by the currents flowing through the canyon (Allen et al., 2001); In the Monterey Canyon, interaction between currents and bottom topography was reported to have a strong impact on the spatial distribution of phytoplankton. Internal tidal pumping of nutrients and resting stages of phytoplankton (i.e. cysts) from the deep shelf and/or canyon to the shallow euphotic zone resulted in local phytoplankton production at the surface. The upsurge of a wedge-shaped tongue of cold, dense water from the canyon was also reported to occur in this canyon, flowing up onto the continental shelf. The intruding water mass was observed to entrain a plume of nutrient-rich turbid water from the seafloor up to the surface, above which high concentrations of phytoplankton were observed (Ryan et al., 2005; 2010). The topographic complexity of canyons, the time-varying nature of currents, and the difficulty in sampling dynamic biological populations in such dynamic environments, makes it

37 Chapter 1 difficult to fully understand the trophic relationships within canyons (Bosley et al., 2004). More direct, interdisciplinary and temporal measurements are necessary to understand the nature of such interactions (Hickey, 1995; Jordi et al., 2008).

1.3. The study area

Central Portuguese margin

In comparison to the larger part of the European Margin, the central Portuguese margin has a relatively narrow shelf (20–50 km wide and a gradient of <1°), passing into a steep irregular slope (6–7°) below the shelf-break which is located at 160-200 m depth. The margin is dissected by a number of long submarine canyons, of which the Nazaré and Setúbal–Lisbon canyons are the most remarkable (e.g. Vanney and Mougenot, 1981; Mougenot, 1989; Alves et al., 2003). The complex morphology and geology of the margin results from a strong structural heritage from deep variscan structures, later affected by Mesozoic extensional tectonics related to the opening of the North Atlantic, and by Cenozoic compression resulting from the collision of the European and African plates. Since the Miocene, the northern margin has experienced major subsidence, which allowed the build-up of thick prograding sedimentary series, particularly on the shelf and slope. The shelf is composed of thick Cenozoic carbonate and detritic formations, filling structural basins formed during earlier rifting phases (e.g. Vanney and Mougenot, 1981; Rodrigues, 2004; Alves et al., 2003). Surface sediments on the shelf are generally very coarse and sand-dominated, and include old littoral deposits formed during the Holocene transgression preserved at shallow water depths. Finer-grained sediments generally increase with depth on the shelf, but also occur in muddy deposits located off the estuaries, in structural depressions at the middle shelf and in the canyons upper reaches. At present, terrigenous sediment supply to the margin is relatively limited, especially since the major rivers Tejo, Douro and Minho have been extensively dammed over the past decades (Dias et al., 2002). Still, it is subjected to the discharge of the more important Portuguese rivers, as well as to a seasonally highly energetic regime (waves and tides). Cliff and beach erosion, reworking of shelf deposits and biogenic production constitute additional sources of sediment (Dias, 1987; Van Weering et al., 2002; Oliveira et al., 2002; 2007). Further down in the continental slope, sediments change from slightly coarser and compositionally variable on the upper slope towards more uniform fine-grained and carbonate- richer hemipelagic muds on the deeper slope (De Stigter et al., 2007; 2011). Surface water circulation along the Portuguese margin is directly dependent on two major current systems that transport surface water masses from west to east across the Atlantic: the North Atlantic Current and the Azores Current south of Iberia (Saunders, 1982; Pollard and Pu, 1985; Barton, 2001; Peliz et al., 2005), both smoothly feeding into the near-surface equatorward flow of the Portugal and Canary currents (Saunders, 1982; Barton, 2001). Underneath, the Iberian Poleward Current (IPC) can be recognized traveling poleward, counter to the general

38 General Introduction circulation and closely bound to the continental slope. This current is mostly restricted to the subsurface layers along most of the eastern subtropical gyre, but it surfaces whenever the Trade Winds weaken or turn northward (Barton, 2001) (see Figure 1.7). Circulation over the Portuguese shelf and upper slope displays a marked seasonal variation: during summer, the Azores high pressure system migrates towards the central Atlantic, typically inducing Trade Winds to become northerly, inducing the upwelling of colder, less salty and nutrient enriched subsurface water to rise to the surface along the Portuguese coast (e.g. Fiúza, 1983; Haynes et al. 1993; Barton, 2001; Relvas et al., 2007; Alvarez et al., 2011); during winter, the Iceland low pressure system intensifies and the dominant wind regime becomes southerly along the western Portuguese margin, inducing the IPC to rise over the upper slope and shelf and resulting in downwelling conditions over the shelf (Fiúza, 1983; Vitorino et al., 2002). Typical winter wave conditions are swells from NW and SW with significant wave heights of 3–4 m, often exceeding 5 m during stormy periods, whereas during summer, a low energy wave regime occurs, reaching mean significant wave heights <2 m (Vitorino et al., 2002). River runoff is an important feature of the winter circulation over the western Portuguese margin. Significant discharge particularly from the NW Portuguese rivers (Mondego, Douro, Minho, Lima, Vouga) results in the formation of low salinity water lenses in the coastal ocean (Peliz et al., 2005). The upper 500 m of water column off Portugal is mostly constituted by the Eastern North Atlantic Central Water (ENACW), which is the main source of the nutrient-rich upwelled waters on the Portuguese coast, and reveals two main components of different origin, converging to this region (Fiúza, 1984; McCave and Hall, 2002): a lighter, relatively warm and salty subtropical branch (ENACWst) formed along the Azores Front, which gradually loses its characteristics as it travels further northwards along the Iberian margin; a less saline colder water mass of subpolar origin (ENACWsp) slowly flowing southwards below the poleward subtropical branch (Fiúza et al., 1998). Underneath the ENACW a strong salinity gradient is noticed down to the core of the Mediterranean Outflow Water (MOW) lying at ~800–1400 m depths (see Figure 1.7). The deeper water masses below the MOW comprise the Northeast Atlantic Deep Water (NEADW) below 2000 m, and the Lower Deep Water (LDW) at levels < 4000 m (Van Aken 2000ab).

Nazaré and Lisbon-Setúbal Canyons

The Nazaré and Lisbon-Setúbal canyons are the largest submarine canyons of the central Portuguese margin, extending from near the shore to abyssal depth (Figure 1.7), and acting as preferential dispersal pathways of particulate matter and attached pollutants from the coast to the deep sea (De Stigter et al., 2007; 2011; Richter et al., 2009; Jesus et al., 2010; Martin et al., 2011). Their morphology, sedimentary processes and impact on the biological communities have been described in recent literature (e.g. Van Weering et al., 2002; De Stigter et al., 2007; 2011; Oliveira et al., 2007; Arzola et al., 2008; Lastras et al., 2009; Garcia et al., 2007; 2010;

39 Chapter 1

Martin et al., 2011; Masson et al., 2011; Koho et al., 2007; 2008; Tyler et al., 2009; Cunha et al., 2011; Mendes et al., 2011), following extensive research performed in the framework of several scientific projects, both Portuguese (i.e. SEPLAT, 1974-2005; DEEPCO, 2006-2009) and European (OMEX II, 1997-2000; EUROSTRATAFORM, 2002-2005; HERMES, 2005- 2009; HERMIONE, 2009-2012). The present morphology of the Nazaré and Lisbon-Setúbal canyons results from erosive processes occurring at least since the middle Miocene. Their location appears to be, at least in part, controlled by the geological structure of the Portuguese Margin. The NE-SW general orientation of the canyons is roughly parallel to pre-existing faults of late-Variscan age, both onshore and offshore (see Vanney and Mougenot, 1990; Alves et al., 2003; Lastras et al., 2009). Such faults represent areas of relative weakness on the slope, thus susceptible to be eroded by

Figure 1.7 - Geographical location of the central Portuguese margin and the Nazaré, Cascais and Lisbon- Setúbal submarine canyons. (a) Schematic map of the central Portuguese margin, showing the Nazaré, Cascais and Lisbon-Setúbal submarine canyons, and the most important features of oceanic circulation off Portugal. Arrows represent the main currents: summer equatorward shelf current (continuous blue), IPC (continuous red), Portugal Current (thick grey), ENACWsp and ENACWst (short dashed), and MOW (thick green). IAP and TAP refer to the Iberian and Tagus Abyssal Plains, respectively.

gravity flows, and leading to the progressive headward erosion of the canyons (Pratson and Coackley, 1996; Arzola, 2008). The presence of large sedimentary levees along the lower course of the Nazaré and Setúbal canyons indicates that the two canyons acted as conduits for large-scale sediment

40 General Introduction transport to the deep-sea, contributing turbiditic sediments to the Tagus and Iberia Abyssal Plains, at least since the Miocene. Sediment core analysis indicates that highest sedimentation rates in this area mostly occurred during sea-level low stands of glacial times (Arzola et al., 2008). Turbidity currents were the dominant processes of sediment erosion, transport and deposition in the two canyons during glacial times. Closely-spaced stacks of thin turbidite layers that are commonly observed in late-glacial deposits from the lower canyon are thought to be generated by fluvial processes directly affecting the upper canyons. Larger-volume canyon- flushing events triggered by earthquakes were relatively less common during glacial periods. During the Holocene, little sediment appears to have reached the abyssal plain through the canyons with their upper and middle sections acting as sediment morphological traps, as revealed by exceptionally high sedimentation rates recorded in these regions (De Stigter et al., 2007; 2011; Masson et al., 2011; Martin et al., 2011). Nevertheless, the Nazaré and Lisbon- Setúbal canyon still exhibit a certain degree of activity, mostly controlled by internal tidal dynamics and sediment gravity flows triggered by meteorological forcing (Oliveira et al., 2007; De Stigter et al., 2007; 2011; Martin et al., 2011). The present-day activity appears different for the two canyons, probably related to their different geographical setting and morphology. The Nazaré Canyon is one of the largest and deepest submarine canyons of the European Margin, cutting across the full width of the central Portuguese margin, with its head located at ~50 m water depth and less than 1 km from the shore. Although it is presently not connected to a major modern drainage system, it is recognized as a major sediment pathway among European canyons, obtaining its sediment input by capture of particles transported by littoral drift (Duarte et al., 2000) and along the shelf (Oliveira et al., 2007; De Stigter et al., 2007). In the upper and middle parts of the Nazaré Canyon, sediments are continuously resuspended and transported by strong internal tidal currents, as reflected by high turbidity values in bottom waters (up to 300 m above the bottom), high horizontal and vertical sediment fluxes in the bottom water layer. The diminishing strength of tidal currents down-canyon results in focused sediment deposition in the middle canyon, as revealed by high sediment accumulation rates observed in sediment traps and sediment cores in that area (De Stigter et al., 2007; Masson et al., 2011) (Figure 1.8). Transport of fine-grained sediments further down to the lower canyon occurs through the action of intermittent gravity-driven flows triggered by resuspension of shelf sediments by winter storms and enhanced input of sediments by the flooding of rivers north of the canyon and around the canyon head. The deep indentation of the canyon into the coastline and high exposure to incoming westerly storms certainly contributes to enhanced sediment input (Oliveira et al., 2007; De Stigter et al., 2007; Martin et al., 2011; Masson et al., 2011). Transport of coarser sand-sized material to the lower canyon only occurs in centennial or longer time scales, with the most recent turbidite layer found in this region interpreted as representing a canyon-flushing event triggered by the 1755 AD Lisbon Earthquake (Figure 1.9) (De Stigter et al., 2007). Despite of the apparently less energetic environment in the lowermost part of the canyon at the present, coarse gravel exposed in the canyon walls indicates a much more active dynamics in the past, with catastrophic processes capable of transporting boulders up to 1 m across (Tyler et al., 2009).

41 Chapter 1

Although connected with two major river systems, i.e. Tagus and Sado rivers, the Lisbon- Setúbal Canyon appears to be much less dynamic than Nazaré Canyon, and presently inactive in terms of down-canyon mass sediment transport (De Stigter et al., 2011). Unlike the Nazaré Canyon, gravity-driven sediment flows appear rare at present in the Lisbon-Setúbal Canyon. In addition, an overall up-canyon flow was observed to produce a net transport of suspended sediment toward the canyon head rather than disperse sediment down-canyon. In the middle and lower parts of the canyon, the sediment is essentially hemipelagic, similar to the sediment found on the adjacent continental slope (De Stigter et al., 2011). The location of the heads of the Lisbon and Setúbal canyon branches at somewhat deeper water a few km off the coast, and the relatively sheltered position of the upper canyon behind prominent coastal capes, probably contribute to its low present-day sedimentary activity. During sea-level low-stands, however, the heads of the Lisbon and Setúbal canyon branches were probably indenting the estuaries of the Tagus and Sado rivers (Dias et al., 2000), thereby funneling large amounts of sediments to the deep-sea through high-energy and erosive turbidity currents similar to those reported from the Nazaré Canyon (Arzola et al., 2008; Lastras et al., 2009).

Figure 1.8 - Suspended particle load above the seabed in the axis of Nazaré Canyon (Tyler et al., 2009).

Little is known yet about the influence of the central Portuguese canyons on the productivity and distribution of phytoplankton assemblages. The focus of biological research in these canyons has been directed at understanding the functioning of benthic ecosystems, related to the fact that the canyons are recognized as major temporary depocenters and conduits of organic-rich particles to the deep-sea (Garcia and Thomsen, 2008; Masson et al., 2010; Garcia et al., 2010), and sites of high heterogeneity in terms of substrate and physical processes. The Portuguese canyons appear to have an important role in modifying abundance and diversity patterns that are normally observed in continental slope environments (Cunha et al., 2011). A large variety of faunal species was observed in the Nazaré Canyon by Tyler et al. (2009), suggesting the canyon represents a biodiversity hotspot. However, lower abundance of meiobenthos observed along the axis of the upper Nazaré Canyon by Koho et al. (2007, 2008)

42 General Introduction

Figure 1.9 – Sediment core collected from the lower Nazaré Canyon, at 4976 m depth, showing a 19 cm thick turbidite layer at its base, resulting from a canyon-flushing event triggered by the 1755 AD Lisbon (De Stigter et al., 2007).

and Garcia et al. (2007) was interpreted to result from the prevailing strong bottom currents and unstable sedimentary conditions, whereas higher abundances on the sediment-draped terraces and further downslope on the flat-floored middle and lower canyon sections (3000–5000-m water depth) suggest that benthic organisms actively profit from fresh organic matter that is episodically flushed from the upper canyon and deposited there (Koho et al., 2007; Garcia et al., 2007). High abundance coupled with low biodiversity was also observed in macrofauna from the upper part of Nazaré and Lisbon-Setúbal canyons in comparison to the adjacent slope regions (Cunha et al., 2011). Mendes et al. (2011) performed the first investigation on the distribution and composition of phytoplankton assemblages in the Nazaré Canyon, during an upwelling event, on the basis of phytoplankton pigments. According to these authors coccolithophores appeared most common outside the upwelling areas, in stratified and nutrient-poor waters. Maximum values of 19’ hexanoyloxyfucoxantine, a pigment that represents a proxy for coccolithophores, were noticed north of the canyon and the maximum concentrations of phytoplankton biomass (i.e. Chl-a were found in the inner shelf north of the canyon’s head. The other two dominant phytoplanktonic groups – diatoms and dinoflagellates – were more abundant in nutrient-rich upwelled waters along the coast. Contrasting nutrient conditions north and south of the canyon were interpreted as resulting from the interaction between the canyon topography and upwelling currents, in particular the intensification of upwelling in the canyon head and southern canyon rim and nearby shelf.

43 Chapter 1

1.4. Framework and Objectives of the Thesis

The central Portuguese Margin and the Nazaré and Lisbon-Setúbal canyons have been the subject of studies carried out in the framework of several scientific projects over the past decades. The SEPLAT1 national program (1974-2005) was designed and developed by the Portuguese Hydrographic Institute with the purpose of identifying the nature and extension of the sedimentary deposits offshore Portugal and to produce the cartographic map of the superficial sediments from the Portuguese Continental Shelf, at 1:150,000. Over 12600 sediment samples were collected in the course of around 30 hydrographical cruises, providing the fundamental basis of several research studies and training in the course of the last decades (Bizarro, 2010). The OMEX-I1 (1993-1996) (Wollast and Chou, 1996) and OMEX-II1 (1997– 2000) (Van Weering and McCave, 2002) projects, investigated the exchange of particulate and dissolved matter, with special focus on the exchange of organic carbon across the continental margin of, respectively, the northern Bay of Biscay and NW Iberia. Some work was dedicated to the Lisbon Canyon (Jouanneau et al., 1998) and Nazaré Canyon (Van Weering et al., 2002). The EUROSTRATAFORM project1 (2002-2005) (Weaver et al., 2006) was more directly focused on exploring the role of canyons as preferential conduits of sediment transport to the deep ocean, using among others the Nazaré and Lisbon-Setúbal canyons as examples of contrasting sedimentary systems (Weaver, 2006). The DEEPCO1 national project (2006-2009) aimed to investigate the geomorphological, geophysical, sedimentary features of the submarine canyons dissecting the NW Portuguese continental shelf, notably the Porto, Aveiro and Nazaré canyons (Guerreiro et al., 2005-2006). More recently, the projects HERMES1 (2005-2009) (Weaver and Gunn, 2009) and HERMIONE1 (2009-2012) (Weaver et al., 2009) had a broader multidisciplinary approach, covering geology, oceanography and biology. The main purpose of these projects was the mapping and understanding of the marine ecosystems on the European continental slope, including man’s influence on these ecosystems. A very significant amount of oceanographical, geological and biological data was acquired from the two canyon systems during these projects, much of which has been published in recent literature. As the Portuguese canyons were found to constitute major temporary traps of organic- rich sediment (see Van Weering et al., 2002; De Stigter et al., 2007; 2011), most biological studies were directed at the benthic ecosystems profiting of organic matter enrichment (e.g. Koho et al., 2007; 2008; Garcia et al., 2007; Amaro et al., 2009; Tyler et al., 2009; Cunha et al., 2011). Little attention was given to the phytoplankton communities thriving in these regions. The main purpose of this thesis consists in filling this gap, focusing on the coccolithophores. The central hypothesis of this thesis, supported by field observations and results from

1 SEPLAT – Carta dos Sedimentos Superficiais da Plataforma Continental Portuguesa; DEEPCO – Deep Sedimentary Conduits of the West-Iberian Margin; OMEX – Ocean Margin Exchange; EUROSTRATAFORM – European Strata Formation; HERMES – Hotspot Ecosystem on the Margins of European Seas; HERMIONE – Hotspot Ecosystem Research and Man’s Impact On European Seas.

44 General Introduction numerical models, is that enhanced coast-shelf-slope exchange within submarine canyons is capable of affecting the dynamics of plankton ecosystems (see Hickey, 1995; Kampf, 2006; Skliris et al., 2002; Bosley et al., 2004; Skliris and Djenidi, 2006; Ryan et al., 2005; 2010). The present dissertation aims to (a) investigate the effects of the central Portuguese canyons on the ecology of recent coccolithophores, along coast-ocean transects, along and outside the canyons, (b) explore the potential of coccoliths as tracers of oceanographic processes occurring at the central Portuguese margin, namely those related to the submarine canyons. In order to achieve this, water column and surface sediment samples were analysed to study the coccolithophore living communities (i.e. biocoenosis) and sub-fossil coccolith assemblages (i.e. thanatocoenosis), respectively. Data obtained from the water column and surface sediment are compared and integrated within a multidisciplinary and multi-proxy approach. Particular focus is attributed to the Nazaré Canyon.

In more specific terms, the present study aims to address:

(1) the coccolithophore assemblages currently thriving in the Nazaré Canyon region, and the ecological preferences and spatial (lateral and vertical) distribution of individual taxa; (2) the relationship between the ecology of coccolithophores and the environmental (meteorological and hydrographical) settings off central Portugal; (3) the potential role of the Nazaré Canyon topography on the distribution, productivity and ecology of living coccolithophores; (4) the (paleo)ecological and (paleo)oceanographical differences between the Nazaré and the Lisbon-Setúbal canyons, and between the canyons and their adjacent shelf-slope regions; (5) the extraction of the (paleo)ecological signal within the coccolith sediment assemblages, independent from the intensified taphonomical effects in submarine canyons and coastal settings; (6) the introduction of Compositional Data Analysis (i.e. the isometric log-ratio approach) as a new procedure to validate and obtain consistent (paleo)ecological interpretations.

1.5. Outline of the Thesis

This study presents data on living coccolithophore concentrations (cells per litre) from surface waters of the Nazaré Canyon region, collected during a late winter period, and coccolith species concentrations (nanno per gram of sediment) obtained from surface sediments collected over a wider area in the central Portuguese margin, including the Nazaré, Lisbon-Setúbal and Cascais canyons, and their adjacent shelf-slope areas off Cape Mondego, Estremadura spur and off Cape Sines. The complete list of samples, respective positions, depth and analysed proxies is presented in Appendix D. Results are integrated and discussed within a significant and

45 Chapter 1 multidisciplinary data set concerning the ecological and hydrological late-winter characteristics off central Portugal, and topographic and sedimentological features of the seabed. In Chapter 2, a general characterization of the late winter coccolithophore communities thriving in the Nazaré Canyon region is presented. Hydrographic and meteorological variability during the winter-spring transition are taken into consideration while interpreting the ecological preferences of coccolithophores. The impact of short-term environmental changes on the productivity and ecology of this group, and the rapid response of certain species to nutrient input, are investigated and discussed. In Chapter 3, the impact of the Nazaré Canyon topography on the spatial distribution and ecological preferences of the late winter coccolithophore assemblage is investigated, whereas the potential of certain species as tracers of oceanographic phenomena occurring in the canyon during this time of the year is explored. Results presented here are part of the ongoing investigation by the Portuguese Hydrographic Institute of the complex dynamics of the Nazaré Canyon (biological, physical and sedimentary), in relation with the seasonal circulation pattern prevailing west of central Portugal. Chapter 4 deals with the coccoliths preserved in surface sediment samples from the central Portuguese margin. North-South and onshore-offshore trends in coccolith concentrations and species percentages were analysed in relationship with sediment characteristics (i.e. sediment bulk composition, particle size, accumulation rate) to investigate to what extent these assemblages reflect a primary ecological signal related to surface water oceanography, and to what extent they are modified by taphonomical processes including reworking by bottom water currents. A comparison is made between the ecological and sedimentary dynamics of Nazaré Canyon and the Lisbon-Setúbal Canyon, and between the canyons and adjacent shelf-slope areas. Chapter 5 is of a more methodological nature; a review of the factors controlling the sedimentation of coccoliths in coastal settings is presented, and the Compositional Data Analysis (CoDA) is introduced as a new statistical tool to study the coccolith assemblages, and to confirm the effect of submarine canyons on the (paleo)ecology of coccolithophores. Results from using CoDA are compared to those obtained from classical analytical methods, (i.e. coccolith concentrations - nanno/g; coccolith fluxes - nanno/cm2/yr; and percentages), and further discussed. Chapter 6 synthesises the results presented in the previous chapters, with the aim of conceiving a general conceptual model for the role of the canyons in the (paleo)ecology and taphonomy of coccolithophores. It includes a qualitative comparison between the living communities and the recent coccolith assemblages preserved on the seafloor. The potential of coccoliths as (paleo)ecological and (paleo)oceanographic proxies in coastal settings and tracers of oceanographic processes prevailing within and around submarine canyons is discussed. Finally, proposals for future research are presented.

46 General Introduction

1.6. Material and Methods

A total of 219 samples were analysed for the study of coccolithophores and coccoliths (see Appendix D). A detailed description of the sampling, laboratory work and microscope analysis used in this study - including the analysis of nutrients, Chl-a concentrations and acquisition of satellite imagery, which were performed by other researchers - is included in each chapter of the thesis, and hence only a brief overview is presented below.

Sampling

127 Water samples were collected at discrete depth levels (between 5 and 110 m depth) from 39 CTD (conductivity, temperature, depth) casts around the Nazaré Canyon region. Sampling was conducted between 9 and 19 of March 2010, on board of NRP “Almirante Gago Coutinho” during the 2nd HERMIONE scientific cruise. CTD profiling and water column samples were collected using a combined Neil Brown MKIIIC CTD profiler equipped with an Aquatracka nephelometer, a Seapoint fluorometer and a rosette sampler (12 Niskin bottles of 8 l) (Figure 1.10). Additional samples were collected to analyse nutrients and chlorophyll-a. 92 Surface sediment samples were taken from the top 0.5 or 1 cm of box- and multicores, collected along six transects crossing the central Portuguese margin in an approximately E-W direction, along the Nazaré and Lisbon-Setúbal canyons and along adjacent shelf and slope areas. Sediment coring was performed during several cruises with RV Pelagia of Royal NIOZ between 2002 and 2011, in the framework of the European projects EUROSTRATAFORM and HERMES, and the Dutch scientific projects ‘‘Lead in Canyons’’ and “Pacemaker” (Figure 1.10).

Laboratory and Microscope Analysis

For the study of coccolithophores, seawater samples of around 2 l were filtered over cellulose acetate filters (47 mm diameter and 0.45 μm pore size) using a low pressure vacuum system. Coccospheres (cells) were identified and counted from a randomly chosen section of each filter, cut and permanently mounted on a glass slidewith a synthetical resin (Entellan), using polarized light microscope (PLM) (Olympus BX-40) at 1250× magnification. The number of cells per liter (cells/l) was estimated according to Cros (2001). To refine the taxonomic differentiation of certain groups, 18 samples were investigated using Scanning Electron Microscope (SEM Hitachi S-3500N, at 5 kV). For the study of sediment coccolith assemblages, a minimum of 300 individual coccoliths were counted and identified from slides previously prepared according to the random settling procedure (Flores and Sierro, 1997), using PLM. To minimize possible bias by differential dissolution, only coccolithophore species producing relatively large and more robust coccoliths (≥ 3 µm) were considered for the (paleo)ecological analysis.

47 Chapter 1

Figure 1.10 – Aspects of the CTD profiler and rosette sampler containing the Niskin bottles (a-b); seawater collection (c) and filtering on the laboratory onboard, using a low pressure vacuum system (d); multicorer equipment and collected sediment multicores (e-h); aspect of the uppermost sediment fluff layer in perfect preservation, representing the water-sediment interface (i).

48 General Introduction

Taxonomic identification of coccolithophores from both seawater and sediment samples was performed according to Jordan et al. (2004). As most of the sedimentological data presented in this thesis have been previously presented and discussed by De Stigter et al. (2007, 2011), Jesus et al. (2010) and Costa et al. (2011), the reader is referred to these authors for a complete description of the analytical methodology used to determine the sediment bulk composition, particle size and sediment accumulation rates.

Statistical analysis

Statistical multivariate analysis (r-mode Factor Analysis, by Statistica 10) and Spearman correlation were used to investigate the relationship between coccolithophore taxa and the environmental conditions. The analyses were performed upon data matrices with coccolithophore data and the associated environmental proxies as columns (variables) Chapters 2, 3 and 4). The isometric log-ratio (ilr) approach of Compositional Data Analysis (CoDA) (Egozcue et al., 2003) was used to test and validate the results obtained from the coccolith percentages (Chapter 5). Six compositional balances were determined by applying a sequential binary partition to seven taxonomic groups, based on our pre-knowledge of their ecological preferences from the scientific literature (e.g. Winter et al., 1994; Cachão and Moita, 2000; Cachão et al., 2000; Silva et al., 2008), and from the species percentages (Chapters 4 and 5). A balance- dendrogram representing the six isometric log-ratios was automatically obtained using CODAPACK software (Version 2.01.13).

49

Chapter 2

Late winter coccolithophore bloom off central Portugal in response to river discharge and upwelling

Chapter 2 Late winter coccolithophore bloom off central Portugal in response to river discharge and upwelling

Published as C. Guerreiro, A. Oliveira, H. de Stigter, M. Cachão, C. Sá, C. Borges, L. Cros, A.I. Santos, J.-M. Fortuño, A. Rodrigues, 2013. Late winter coccolithophore bloom off central Portugal in response to river discharge and upwelling. Continental Shelf Research 59, 65-83

Abstract

Coccolithophore communities collected during late winter (9–19 March of 2010) over the central Portuguese margin showed a major change in species abundance and composition within a few days’ time, closely related to the highly transient meteorological and oceanographic conditions. Particularly favourable conditions for coccolithophore growth resulted from late winter continental runoff combined with northerly winds prevailing over the shelf, under clear sky conditions. A nutrient-rich Buoyant Plume (BP) resulting from intense river water runoff prior to and during the start of the cruise, was observed to spread out over the denser winter mixed layer water beneath, and extend equatorwards and offshore under influence of Ekman superficial dynamics. Stabilization of buoyancy, settling of suspended sediment from the BP and the prevailing clear sky conditions in the transition to the 2nd leg of the cruise resulted in optimum conditions for coccolithophores to develop, at the expense of nutrient availability in the superficial sunlit layer. Within a few days, coccolithophore cell densities and associated phytoplankton biomass more than tripled, reaching maximum values of 145,000 cells/l and ~13 mg/l Chl-a, respectively. Often considered as a uniform functional group of calcifying phytoplankton thriving in low-turbulence, low-nutrients and high-light environments, results presented in this study clearly show that coccolithophore life strategies are much more diverse than expected. The increase of cell densities was mainly due to the bloom of Emiliania huxleyi and Gephyrocapsa oceanica in the coastal region west off Cape Carvoeiro, together with other opportunistic phytoplankton genera (Chaetoceros s.l., Thalassiosira s.l and Skeletonema s.l.). This confirms their role as early succession r-selected taxa, capable of rapid growth within nutrient-rich environments. On the contrary, Syracosphaera spp. and Ophiaster spp. displayed the characteristics of K-selected species, being consistently more abundant in more oceanic and less eutrophic waters, away from the influence of the BP, during both low- and high-productive periods.

53 Chapter 2

A general description of coccolithophore communities as well as the environmental conditions during this period is presented in this study (i.e. hydrography and nutrient availability). Multivariate analysis was used to investigate the impact of short-term environmental changes on the productivity and ecology of this group. In view of the observed dominance of coccolithophores off Portugal during winter, this transitional period appears particularly favourable for coccolithophores to develop. The results highlight the importance of taking short-term hydrographic and meteorological variability into account when interpreting the ecological preferences of coccolithophores from coastal-neritic-oceanic transitional settings.

Keywords: Coccolithophore ecology; river runoff; Ekman circulation; haline-stratification; Portuguese margin

2.1. Introduction

Coccolithophores are a major group of unicellular marine phytoplankton, representing the main component of extant calcareous nannoplankton. Their ability to produce delicate calcite platelets, the coccoliths, combined with their ocean-wide distribution, makes them the most productive calcifying organisms on Earth, with remarkable potential as paleoenvironmental markers (e.g. Winter et al., 1994; Ziveri et al., 2004; Silva et al., 2008). In addition to their unique role in the marine carbon cycle, forming part of both the biological and carbonate pumps (Rost and Riebesell, 2004), they are likely to produce additional feedback to climate due to their physical (albedo increase resulting from the highly reflective masses of detached coccoliths) and biochemical (production of dimethylsulphonium propionate - DMSP) characteristics (Westbroek et al., 1993; Malin and Steinke, 2004). The general biogeography and habitat characteristics of coccolithophores are known from plankton and bottom sediment surveys (McIntyre and Bé, 1967; Brand, 1994; Roth, 1994; Winter et al., 1994; Young, 1994; Ziveri et al., 2004). The group is usually associated with oligotrophic conditions in warm and stratified waters from low and middle latitude regions (e.g. McIntyre and Bé, 1967; Winter et al., 1994; Ziveri et al., 2004). However, local phenomena such as coastal currents, gyres, eddies, upwelling, river runoff, are known to regionally affect their productivity (Cachão and Moita, 2000; Ziveri et al., 2004). Studies of modern coccolithophores suggest that their ecology is mostly controlled by light and nutrient availability rather than by temperature and water stratification alone. This is indicated by their occurrence in blooms (e.g. Knappertsbusch and Brummer, 1995; Souza et al., 2011) in the context of subtropical oligotrophic gyres or within turbulent coastal and mature upwelled waters (e.g. Ziveri et al., 1995; Baumann et al., 1999; 2000; Cachão and Moita, 2000; Moita, 2001; Moita et al., 2010; Silva et al., 2008). More regional studies on living coccolithophores are required to calibrate their specific local ecological tolerances and to assess their potential for local paleoceanographic reconstructions (e.g. Andruleit et al., 2003).

54 Late winter coccolithophore bloom

The central Portuguese margin (Figure 2.1) is part of the North Atlantic Upwelling Region (see Relvas et al., 2007), and located on the boundary between the transitional and the subtropical coccolithophore biogeographical zones (McIntyre and Bé, 1967). In a number of important studies on the coccolithophore assemblages living off Portugal, the group generally appears to be dominant over diatoms during winter, when warmer and nutrient-depleted subtropical waters flow onto the Portuguese shelf (Abrantes and Moita, 1999; Cachão and Moita, 2000; Cachão et al., 2000; Cachão and Oliveira, 2000; Silva et al., 2008, 2009; Moita et al., 2010). The entrainment of subtropical water masses, originating from south of the Azores Front into the Iberian Poleward Current during winter, is reflected in coccolithophore assemblages by the occurrence of subtropical species like Algirosphaera quadricornu, Alveosphaera bimurata, Cyclolithus annulus, Florisphaera profunda, Michaelsarsia elegans, Syracosphaeara lamina and Turrilithus latericioides, along with temperate species like Gephyrocapsa muellerae, Gephyrocapsa ericsonii and Emiliania huxleyi (Cachão et al., 2000). More recently, during a four years weekly survey, Silva et al. (2008) performed the first systematic investigation of the coccolithophore assemblages from offshore Portugal. This study confirmed the preference of the group for non-upwelling conditions, although certain species appeared capable of withstanding coastal turbulence and well-adapted to the nutrient-rich coastal environment (i.e. E. huxleyi, Gephyrocapsa oceanica). Later, Moita et al. (2010) identified the assemblage composed by Helicosphaera carteri, Syracosphaera pulchra and Coronosphaera mediterranea as a summer tracer of subtropical waters upwelled along the southwestern and southern coast of Portugal. Here we report on coccolithophore assemblages collected during a two-leg hydrographic and plankton survey west off Portugal, during a late winter period (9–19 March 2010) at the end of an exceptionally negative phase of the North Atlantic Oscillation. A detailed characterization of the living assemblages is presented, as well as a general description of the meteorological and oceanographic conditions during the cruise (i.e. wind, hydrography, chlorophyll-a and nutrient availability). Our aim is to investigate the impact of the transient environmental settings on the ecology and productivity of this group in the central Portuguese margin.

2.2. Regional setting

The central Portuguese margin has a relatively narrow shelf (20–50 km wide and a gradient <1º), which at 100–200 m depth passes into a steep irregular slope (6º–7º). The shelf is composed of thick (>1000 m) Cenozoic sediments covering a Mesozoic substrate (Jouanneau et al., 1998) and dissected by a number of long submarine canyons, namely the Nazaré, Cascais and Setúbal–Lisbon canyons (e.g. Vanney and Mougenot, 1981; Alves et al., 2003; Lastras et al., 2009). Surface water circulation along the Portuguese margin is directly dependent on two major current systems that transport surface water masses from west to east across the Atlantic: the North Atlantic Current extending to the north of the Iberian Peninsula, and the Azores Current

55 Chapter 2 south of Iberia (Saunders, 1982; Pollard and Pu, 1985; Barton, 2001; Peliz et al., 2005). As the Azores Current flows eastwards, branches of this current smoothly loop northward into the Portugal Current and southward into the Canary Current (Saunders, 1982; Barton, 2001) (Figure 2.1a). The upper 500 m of water column off Portugal, including the surface mixed layer and the first thermocline, are constituted by Eastern North Atlantic Central Water (ENACW) which is the main source of the nutrient-rich upwelled waters along the Portuguese coast. The ENACW has two main components of different origin, converging to this region: a lighter, relatively warm and salty subtropical branch (ENACWst) formed along the Azores Front, which gradually loses its characteristics as it travels further northwards along the Iberian margin; a less saline colder water mass of subpolar origin (ENACWsp), related to the Subpolar Mode Water formed in the eastern North Atlantic by winter cooling and deep convection (Fiúza et al., 1998), slowly flowing southwards below the poleward subtropical branch (Figure 2.1a). Beneath the near-surface equatorward flow of the Portugal and Canary currents, the Iberian Poleward Current (IPC) can be recognized travelling poleward, counter to the general circulation and closely bound to the continental slope, its core extending about 300–400 m vertically (Figure 1a). This current is mostly restricted to the subsurface layers along most of the eastern subtropical gyre, but it surfaces whenever the Trade Winds weaken or turn northward (Barton, 2001). Circulation over the Portuguese shelf and upper slope displays a marked seasonal variation associated with seasonal shifts in the position of the Azores high and Iceland low pressure systems (e.g. Haynes et al., 1993; Barton, 2001; Relvas et al., 2007). During summer, the Azores high migrates towards the central Atlantic, typically inducing Trade Winds to become northerly, inducing an equatorward circulation over the upper 150–200 m of the water column off Portugal. A surface layer of about 30 m thick of relatively warmer and lighter water is swept offshore by Ekman transport, allowing colder, less salty and nutrient enriched subsurface water to rise to the surface along the coast (e.g. Fiúza, 1983; Haynes et al., 1993; Barton, 2001; Relvas et al., 2007; Alvarez et al., 2011). During winter, when the Azores high is located further south and the Iceland low intensifies, the dominant wind regime becomes southerly along the western Portuguese margin. This induces the IPC to rise over the upper slope and shelf, where the poleward flow produces an onshore Ekman transport, in turn resulting in downwelling conditions over the shelf (Fiúza, 1983; Vitorino et al., 2002). Discharge of fresh water from rivers and streams, leading to the formation of coastal low salinity water lenses, is another important feature of the winter circulation over the western Portuguese margin. The Buoyant Plumes (BP’s) that are thus formed either develop into inshore currents (Relvas et al., 2007; Otero et al., 2008) or spread further offshore, depending on the wind forcing conditions over the shelf (Otero et al., 2008). Under typical winter conditions, the onshore Ekman transport driven by prevailing southerly winds induces the saline front to move toward the coast, thus forcing the BP to develop into a narrow coastal current with strong poleward velocities (e.g. Marta-Almeida et al., 2002; Oliveira et al., 2002; Relvas et al., 2007). When the southerly winds weaken or turn northerly, offshore spreading of the plume occurs,

56

Figure 2.1 – (a) Schematic map of the central Portuguese margin, showing topographic features and surface and deep currents mentioned in the text. Rectangle indicates the sampling area. Arrows represent the main currents: river runoff (thick brown) and offshore and equatorward expansion of the buoyant river plume (curved brown dashed lines), summer equatorward shelf current (continuous blue), IPC (continuous black), Portugal Current (thick light grey), ENACWsp and ENACWst (short dashed), and MOW (long dashed); (b) Enlargement of the sampling area. Black squares and triangles refer to CTD casts from the 1st and 2nd legs (March, 2010), respectively. Green squares refer to stations where samples were collected for HPLC. Squares with a black contour refer to stations where samples were collected for nutrient analysis. Stations with number label indicate the locations where coccolithophore sampling was performed. Red and blue lines represent the location of the density profiles along the upper-middle Nazaré Canyon axis and west of Cape Carvoeiro, during the 1st and 2nd legs of the cruise, respectively, as shown in Figure 2.3.

Chapter 2 even when wind variation is of short (1–3 h) duration (Otero et al., 2008) (Figure 1a). The Western Iberian Buoyant Plume is mostly fed by outflow from the northern Portuguese rivers (Mondego, Douro, Minho, Lima, Vouga), and is characterized by low salinities (<35.8) and lower temperature than the ambient shelf waters (Peliz et al., 2005). The seasonally variable circulation on the Portuguese shelf and slope is also subject to interannual variation associated with the North Atlantic Oscillation (NAO), the latter resulting from fluctuations in the difference of atmospheric pressure between the Azores high and the Iceland low. Under NAO high index conditions, Trade Winds increase and bring moist air to Europe, leading to cool summers and mild and wet winters in central Europe and its Atlantic facade. On the contrary, NAO low index conditions are characterized by atmospheric temperature extremes with heat-waves and cold spells, and an increase of storm activity and rainfall in southern Europe and North Africa. Several studies indicate that in more recent years upwelling events off Portugal have decreased in intensity but increased in frequency, occurring even during the winter period (e.g. Barton, 2001; Vitorino et al., 2002; Santos et al., 2004; Ribeiro et al., 2005; Silva et al., 2008; Alvarez et al., 2009), apparently linked with the trend toward the “high index” polarity of the NAO observed over the last decades, (Barton, 2001; Wallace, 2002).

2.3. Material and methods

2.3.1. Sample collection

Sampling was conducted between 9 and 19 of March 2010, on board of NRP “Almirante Gago Coutinho” during the 2nd HERMIONE (Hotspot Ecosystem Research and Man’s Impact on European Seas) scientific cruise. Coccolithophore communities were investigated in 127 water column samples collected and analyzed from 39 CTD (conductivity, temperature, depth) casts from the Nazaré Canyon region (Figure 2.1b, Appendix D). Samples were collected at discrete water depth levels between 5 and 110 m depth to assess the distribution of coccolithophores along the shelf and oceanic water column in relation with hydrographic and biological characteristics. During the 1st leg (9–12 March) CTD profiling and water sampling was conducted along a transect in the upper and middle part of Nazaré Canyon following the canyon axis, as well as along transects across the upper canyon and surrounding shelf. During the 2nd leg (15–19 March) profiling and sampling was conducted along a transect crossing the Nazaré Canyon near the upper-middle canyon transition (stations 174, 176 and 258), and two transects across the adjacent shelf and slope, one along the northern valley, a minor incision of the shelf break north of Nazaré Canyon (stations 146, 142 and 251), and the other west off Cape Carvoeiro, south of the canyon. Physical oceanographic, biological and chemical data (i.e. temperature, salinity, turbidity, fluorometry and nutrients) and water column samples were collected using a combined Neil

58 Late winter coccolithophore bloom

Brown MKIIIC CTD profiler equipped with an Aquatracka nephelometer, a Seapoint fluorometer and a rosette sampler (12 Niskin bottles of 8 l). Around 192 samples of suspended matter were collected from surface, intermediate and bottom nepheloid layers in order to define the particulate matter concentration and to calibrate the nephelometer response (turbidity). Calibration of turbidity was carried out following the manufacturer's recommendations. The used nephelometer has a pulsed Xenon flash light source with high ultra violet content (440 nm), and measures light scattered back from suspended particles using a solar-blind photodiode detector. It has a very high sensitivity to low values of turbidity, and to small particles (<4 mm), with a precision of 4 % of the measured value. Measurements are not affected by Chl-a (680 nm). The particulate matter concentration (PCM, g/m3) was compared to a laboratory calibration of the instrument with a standard formazine solution (FTU). The turbidity calibration for March 2010 was FTU=0.112×PMC with r=0.88. CTD data are represented as contour plots constructed with the inverse distance to power gridding method of Surfer Version 8.

2.3.2. Meteorological and hydrographic data

Wind data were collected with an Aanderaa AWS 2700 coastal weather station located at Ferrel and maintained by the Portuguese Hydrographic Institute (IH) (position: 39º 23.3’N; 09º 17.5’W, WGS84). Sea wave conditions were obtained from the MONICAN multiparametric buoy (IH) located offshore in the Nazaré Canyon axis (position: 39º 28’N; −9º 40’W) (http://monican.hidrografico.pt/). Average daily river discharge data (m3/s) of the Douro River, measured at the hydrometric station at Crestuma (EDP) (position: 41º 04’N; 8º29’W) were obtained from the Sistema Nacional de Informação de Recursos Hídricos, SNIRH, from Instituto da Água (http://snirh.pt). Photosynthetically Active Radiation (PAR) and monthly averaged chlorophyll-a data (Chl-a) for the area and time interval involved in this study were downloaded from the Ocean Colour Website (http://oceandata.sci.gsfc.nasa.gov). These data were acquired by the Moderate-resolution imaging spectroradiometer (MODIS) on NASA’s Aqua satellite and processed by the Ocean Biology Processing Group (OBPG). Daily images covering the region of interest were averaged for PAR. Cloud coverage was also estimated from MODIS data, as the percentage of pixels in the image flagged with “probable cloud or ice contamination”.

2.3.3. Laboratory and microscope analysis

2.3.3.1. Phytoplankton pigments and nutrients

Chlorophyll-a (Chl-a) concentrations were used as an indicator for phytoplankton biomass. Water samples of 2 l were filtered over Whatman GF/F filters (0.7 μm pore size, 25 mm diameter), and the filters were immediately deep-frozen and stored at −80 ºC. Phytoplankton pigments were extracted with 2–3 ml of 95 % cold buffered methanol (2 %

59 Chapter 2 ammonium acetate) and analyzed with high-performance liquid chromatography (HPLC). Chromatographic separation was carried out following Zapata et al. (2000). Chl-a concentrations obtained from 38 HPLC samples were then used to calibrate fluorometry measurements obtained from CTD casts (r2=0.7 and r2=0.6, with p <0.01, for the 1st and 2nd leg, respectively). Further details on the HPLC method used can be found in Mendes et al. (2007). Water samples for nutrient analysis were filtered on board ship by vacuum with polycarbonate filters of 0.45 mm pore size and kept frozen below −20 ºC until analysis. Nutrient concentrations (NOx: nitrate/nitrite, ammonium, PO4: phosphate, and SiO2: dissolved silica) were determined using a Skalar SAN plus Segmented Flow Auto Analyzer specially designed for the analysis of saline waters. N–NOx and N–NO2 were determined according to Strickland and Parsons (1972), with N–NO3 being estimated by the difference between the previous two;

N–NH4 and Si–SiO2 were determined according to Koroleff (1976); P–PO4 was determined according to Murphy and Riley (1962). All methods were adapted to the methodology of segmented flow analysis and uncertainties were determined following Mendes et al. (2011). Limits of quantification and detection (=1/3 LQ) were, respectively, the following: 0.50 and 0.17 for nitrate+nitrite, 0.1 and 0.033 for nitrite, 1.0 and 0.33 for ammonia, 0.2 and 0.067 for phosphate, and 0.3 and 0.1 for silica.

2.3.3.2. Coccolithophores

For the study of coccolithophores, seawater samples of around 2 l were filtered over cellulose acetate filters (0.45 μm pore size, 47 mm diameter) using a low pressure vacuum system. The filters were then rinsed with tap water to remove salt and oven-dried at 40 ºC for 24 h. A randomly chosen section (approx. 30º–45º) of each filter (radius of ~24 mm) was cut and permanently mounted on a glass slide. Coccospheres (cells) were identified and counted under polarized light microscope (PLM) (Olympus BX-40) at 1250× magnification. The examined area per filter varied between 3.0×105 and 3.4×106 mm2, depending on the general cell density. The number of cells per liter (cells/l) was estimated from the number of counted coccospheres in the examined area multiplied with the ratio of total filter area to examined area and divided by the volume of filtered water (Cros, 2001). Taxonomy of coccolithophores was performed according to Jordan et al. (2004). To refine the taxonomic differentiation of Syracosphaera spp., Gephyrocapsa spp., Algirosphaera robusta and Ophiaster spp., 18 samples were investigated using the Scanning Electron Microscope (SEM Hitachi S-3500N, at 5 kV). Samples were selected for containing relatively higher cell densities and species diversity. A randomly chosen section of the selected filters was fixed with colloidal Ag on a SEM stub and sputtered with an Au–Pd coating of maximum 20 nm thick. A minimum of 100 vision fields (VF) were then examined and coccospheres counted using magnifications between 1000× (observation area of each VF: 1.2×104 μm2) and 2000× (observation area of each VF: 3.0×104 µm).

60 Late winter coccolithophore bloom

2.3.4. Statistical analysis

In order to investigate the relationship between coccolithophore taxa and environmental conditions during the cruise, a statistical multivariate analysis (r-mode Factor Analysis, by Statistica 10) was performed upon data matrices with coccolithophore cell densities, nutrient concentrations (NOx, PO4 and SiO2), Chl-a and physical parameters (temperature, salinity and turbidity) as columns (variables). In view of the very different conditions encountered during the 1st and 2nd leg (see Section 2.4.1) the two legs of the cruise were analyzed separately from two distinct data matrices. Only the more abundant coccolithophore species were considered (>2000 cells/l). Results from the original data matrices were optimized through Varimax Raw rotation.

2.4. Results

2.4.1. Environmental conditions during the cruise

Hydrographic profiling and plankton sampling took place at the end of what for southwest European standards was an unusually cold winter (2009–2010), associated with an exceptionally negative phase of the North Atlantic Oscillation (NAO) (Cattiaux et al., 2010; Troupin and Machin, 2012), as indicated by data from the NOAA-AVHRR data centre (http://www.knmi.nl/datacentrum/satellite_earth_observations/NOAA/2010). Whereas the winter mixed layer still comprised the upper 150–200 m of the water column over the shelf and upper slope, the period of sample collection was marked by transient meteorological and hydrographic conditions. During the 1st leg of the cruise, the general circulation on the shelf was under the influence of intense river runoff, and intensified onshore oceanic convergence induced by the southerly wind regime prevailing prior to the cruise (Figure 2.2). Hydrometric stations along the Douro River measured a peak discharge two weeks prior to the cruise. A shift to northerly winds occurred on the 9th of March 2010, coinciding with the start of the cruise. Initially alternating in northerly and southeasterly direction during most of the 1st leg, the wind increased in strength (max. ~15 m/s) and became persistently northerly in the interval between the two legs, turning back to southerlies on the 15th of March at the start of the 2nd leg (Figure 2.2). Sea wave conditions were mostly moderate, dominated by significant wave heights (Hs) between 1.4 and 2.3 m, mainly coming from W to NW. Ocean colour satellite images indicate a cloud coverage >50 % during most of the cruise except at the end of the 1st leg and the two following days when skies were generally clear. The clear skies resulted in a relative increase of Photosynthetically Active Radiation (PAR) in this short period (Figure 2.2). During both legs of the cruise a well-established surface layer of less dense water was observed, with markedly lower temperature and salinity than that of the underlying winter mixed layer. The layer, interpreted as a buoyant plume (BP) resulting from the recent high river discharge, extended from near the coast to more than 50 km offshore (see water density profiles in Figure 2.3a,b). During the 1st leg, while there was still important river discharge to the shelf,

61 Chapter 2

Figure 2.2 – Time series of relevant meteorological parameters and Douro River discharge measured in March 2010. Mean Photosynthetically Active Radiation (PAR, Einstein/m2/day) and cloud cover (%) determined from satellite imagery. Douro River daily average discharge (m3/s) from the Crestuma (EDP) hydrometric station. Wind intensity (m/s) and direction from the coastal meteorological station at Ferrel. Northerly winds dominated from 9 to 15 of March, later changing to southerlies from 16 to 19 of March of 2010. Grey shaded areas mark the periods of the two legs of the cruise.

T and S values in the BP were conspicuously low (min. 14.2 ºC and 33.8, respectively), slightly increasing during the 2nd leg (min. 14.4 ºC and 34.8, respectively), following three days of persistent northerly wind. Significant variability in thickness of the BP and in the steepness of the TS gradient at its base was noticed during both legs of the cruise. During the 1st leg, closer to the coast, the BP was 40–50 m thick and gradually increasing in TS from the surface down to the winter mixed layer below, suggesting significant vertical mixing between the two water masses; further offshore, the BP decreased to 15–20 m thick with a relatively steep TS gradient at its base. During the 2nd leg, the BP appeared to have increased in thickness relative to what was observed during the 1st leg, with the TS gradient at its lower boundary extending in some cases to more than 100 m depth, closer to the shelf-break. The BP decreased in thickness and at the same time became more sharply defined in offshore direction, with the thinnest BP occurring at the more distal stations off Cape Carvoeiro. The warmer and saltier winter mixed layer underneath the BP was present in the entire investigated region, at depths generally between 15 and 20 m, and 200 m. Higher TS values close to the shelf-break, at the upper-middle Nazaré Canyon transition, and further offshore along the southern flank of the Nazaré Canyon, trace out the core of the IPC along the upper slope. Further north along the slope around 39.5 ºN, lower TS values indicate mixing of the IPC with colder water masses from north.

62 Late winter coccolithophore bloom

Figure 2.3 – Representative density sections based on CTD casts along two coast-to-ocean transects: (a) WSW – ENE transect along the axis of the upper to middle part of Nazaré Canyon covered during the 1st leg, and (b) W – E transect off Cape Carvoeiro covered during the 2nd leg. Location of the transects is indicated on Figure 2.1b. CTD station positions are indicated by tick marks along the top of the graph. Number labels refer to CTD stations where coccolithophore samples were collected.

The boundary with the colder and less saline superficial layer was particularly well- defined during the 1st leg, when the core of the IPC was centred less than 10 km off the coast. The TS gradient marking the boundary between the BP and the winter mixed water layer appeared less acute in CTD profiles measured during the 2nd leg, suggesting mixing of the two water masses had taken place. Whereas turbidity was generally low during the cruise, some near-shore stations monitored during the 1st leg showed higher turbidity at the surface. Enhanced turbidity was clearly associated with the BP, as the highest FTU values corresponded to the lowest salinity. High turbidity values recorded around 200–300 m water depth in the upper canyon, however, appear to reflect bottom sediment resuspension caused by the canyon's internal tide.

63 Chapter 2

2.4.2. Nutrients

During the 1st leg, highest nutrient concentrations were recorded in the relatively cool and low-saline surface water of the BP, decreasing to lower concentrations in the winter mixed water layer below the surface (Figure 2.4). The decrease with depth was particularly noticeable nd in the case of SiO2. During the 2 leg, nutrient concentrations in the superficial water layer appeared to have significantly decreased, becoming lower than in the underlying water mass. In the deeper water layer nutrients had also decreased but much less than near the surface. The rapid depletion of nutrients from the superficial water layer, and slower decrease in nutrient concentrations below the surface is likely reflecting higher rates of nutrient consumptions by phytoplankton at the surface during this time of the cruise. This is particularly apparent for NOx, but to a lesser degree for PO4 and SiO2. Median+/- standard deviation of NOx/PO4 ratio in superficial water layer was 16.1+/- 2.1 and 3.8+/-3.8 during the 1st and 2nd leg, respectively, close to the 16:1 Redfield Ratio typical for marine waters (Redfield et al., 1963). Lower ratio's nd occurring in samples from the 2 leg suggests that NOx was becoming the limiting nutrient for phytoplankton growth at that time.

2.4.3. Phytoplankton biomass (Chl-a) and coccolithophore cell densities

Phytoplankton biomass (Chl-a) and coccolithophore cell densities (cells/l) drastically increased from the 1st leg (max. <1 mg/l and 4.2×104 cells/l) to the 2nd leg (max. ~13 mg/l and15×104 cells/l). Both were generally higher at the upper part of the water column, associated with the relatively cool and low saline superficial layer, and gradually decreasing with depth (Figure 2.5). The highest Chl-a concentrations and cell densities were found off Cape Carvoeiro and further NW, where the northern valley cuts the shelf-break north of the Nazaré Canyon. Whereas coccolithophore cell densities displayed only a weak positive correlation with phytoplankton biomass and no correlation with nutrients during the 1st leg (Figure 2.6), a strong positive correlation with phytoplankton biomass and a negative correlation with NOx and PO4 was observed during the 2nd leg, reflecting the growth of coccolithophores at the expense of nutrients in the surface water layer (Figure 2.7). Additional pigment data (C. Sá personal communication, data not presented in this study) revealed that coccolithophores and diatoms, constituting the two dominant phytoplankton groups, contributed equally to total Chl-a concentration during the 1st leg, with diatoms being generally more abundant at the surface and coccolithophores in deeper subsurface waters. During the 2nd leg, diatoms were clearly the dominant phytoplankton group and the main contributor to Chl-a production, except further offshore where other groups recorded an increase of their relative abundances (station 251).

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Figure 2.4 – Salinity (PSS-78) and nutrient concentrations (µmol/l) measured in the Figure 2.5 - Coccolithophore cell densities (cells/l) and phytoplankton biomass upper 100 m of the water column during the 1st and 2nd leg of the cruise (light and dark (Chl-a µg/l) in the upper 110 m of the water column, measured during the 1st leg (a) and 2nd leg (b) of the cruise. symbols, respectively).

Figure 2.6 – Scatter plots of phytoplankton biomass (Chl-a, µg/l) and Figure 2.7 - Scatter plots of phytoplankton biomass (Chl-a, µg/l) and nutrient nutrient concentration (NOx, PO4, SiO2, µmol/l) versus coccolithophore cell concentration (NOx, PO4, SiO2, µmol/l) versus coccolithophore cell density nd density (cell/l) measured during the 1st leg of the cruise, showing a weak (cell/l) measured during the 2 leg of the cruise, showing a strong positive positive correlation between coccolithophore cell density and correlation between coccolithophore cell density and phytoplankton biomass, phytoplankton biomass, and no correlation between coccolithophore cell and negative correlation with nutrients (particularly PO4 and NOx). density and nutrients.

Chapter 2

2.4.4. Coccolithophore species diversity and ecological preferences

A total of 35 distinct taxa of coccolithophores (coccospheres) were recognized. 19 species and four genera were identified using PLM whereas an additional Scanning Electron Microscope analysis revealed 14 species belonging to the genera Syracosphaera, Ophiaster, Alisphaera and Acanthoica, and one species of holococcolithophore (for the complete list of taxa, see Appendix A). Of the 35 identified coccolithophore taxa, only 10 reached cell densities of more than 2000 cells/l which we considered as significant for subsequent analysis. Mean and maximum abundances of different taxa during the two legs, as determined from PLM observations, are indicated in Table 2.1. The 10 more significant taxa were (in order of maximum abundance): E. huxleyi, G. ericsonii, G. oceanica, G. muellerae, Syracosphaera spp. (dominated by S. marginoporata), C. mediterranea, Ophiaster spp. (dominated by O. hydroideus), Helicosphaera carteri, Syracolithus dalmaticus and A. robusta. Other plankton groups observed on filters collected during the 2nd leg include diatoms (Chaetoceros sp., Rhizosolenia sp., Skeletonema costatum, Thalassionema sp., Thalassiosira sp.), silicoflagellates (Dictyocha fibula), siliceous Chromista as Meringosphaera sp. and Prymnesium neolepis; and dinoflagellates (Ceratium sp., Protoperidinium sp.), calcareous dinoflagellates (Thoracosphaera s.l.), radiolarians (Sticholonche zanclea), choanoflagellates, tintinnids and foraminifera. The strong increase in coccolithophore abundance observed during the 2nd leg of the cruise was mostly due to a strong increase of E. huxleyi, and to a lesser extent of G. oceanica and C. mediterranea (Figure 2.8). All three species can be characterized as surface dwellers, being consistently more abundant at the surface and gradually decreasing with depth. G. ericsonii and S. dalmaticus had also increased during the 2nd leg, although less strongly in comparison to the previous three species. G. ericsonii revealed a broad vertical distribution during both legs, whereas S. dalmaticus was preferably more abundant at the uppermost 5–25 m (Figure 2.8). G. muellerae, Ophiaster spp. and Syracosphaera spp. kept similar cell densities during both periods, although slightly decreasing their maxima during the 2nd leg. Whereas all three revealed a broad vertical distribution, the latter two can be characterized as distinct subsurface dwellers. H. carteri and A. robusta were generally low abundant during the cruise without a specific water depth preference, although maxima of both were observed in the surface water layer. During both legs, coccolithophore assemblages from the bottom nepheloid layer (BNL) generally appeared to reflect those from the surface water layer, dominated by the more productive surface-dwelling species (E. huxleyi, G. ericsonii, G. oceanica and C. mediterranea) and, to a lesser extend from the subsurface dwelling taxa Syracosphaera spp. and Ophiaster spp. The maximum abundance of H. carteri during the cruise was observed in the BNL of station 93, collected during the 1st leg.

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Table 2.1 – Mean and maximum cell densities of the more important coccolithophore species (>2000 cells/l, observed under PLM), for each sampling period, with water column depth, station and bottom depth for which maximum density was observed. (BNL = bottom nepheloid layer ≤110 m). Minimum and maximum values of cell densities, temperature, salinity, turbidity, fluorometry, Chl-a measured by HPLC, phytoplankton biomass and nutrients (NOx, PO4 and SiO2) for the same set of samples are indicated below.

1st leg: 9 -12 March 2nd leg: 15 -19 March

Bottom depth Taxa Cells/l Depth (m) Station Bottom depth (m) Cells/l Depth (m) Station (m) mean max. mean max.

Algirosphaera robusta 299 2049 5 101 51 290 1418 25 238 54 Coronosphaera mediterranea 707 4536 BNL 94 37 1875 7728 5 146 171 Emiliania huxleyi 9520 26353 5 89 40 37317 132900 5 236 100 Gephyrocapsa ericsonii 2774 7115 BNL 111 62 5197 12096 25 146 171 Gephyrocapsa muellerae 1644 9466 50 98 361 1306 3746 25 251 1589 Gephyrocapsa oceanica 534 3893 15 111 62 2402 11841 15 238 54 Helicosphaera carteri 140 5184 BNL 93 33 174 854 5 238a 38 Ophiaster spp. 1510 5544 25 132 3478 1049 5197 25 238 54 Syracolithus dalmaticus 113 3209 25 115 224 494 2722 5 236 100 Syracosphaera spp. 2447 8951 5 132 3478 2426 8307 100 251 1589 min. max. min. max. Cells/l 3629 42077 7818 144693

Temperature (ºC) 13.9 15.04 14.3 15.1

Salinity (PSS-78) 34.3 36.2 35 36.2

Turbidity (FTU) 0.02 0.19 0.02 0.08

Fluorometry (µm/l) 0.11 1.02 0.1 5

HPLC Chl-a (µm/l) 0.06 0.69 0.67 12.3

Phyto. biomass (Chl-a µm/l) 0.15 0.63 0 12.6

NO (µmol/l) 2.3 9.7 0.4 6.7 x PO (µmol/l) 0.1 0.6 0.1 0.3 4 SiO2(µmol/l) 1.7 10.7 0.3 2.5

Chapter 2

During the 1st leg, higher turbidity at the surface appeared to be caused by suspended sediment load supplied by runoff, whereas during the 2nd leg, turbidity showed a good correlation with Chl-a, suggesting it was then related to enhanced phytoplankton productivity (see Figure A in Auxiliary Material). Coccolithophore assemblages showed considerable variation in abundance and taxonomic composition, not only in time (1st and 2nd leg) and water depth (surface and subsurface layer), but also laterally (near-shore and offshore). As illustrated by Figure 2.9, the large increase in coccolithophore abundance from the 1st to the 2nd leg (from less than 4.3×104 cells/l to more than 14×104 cells/l, respectively) was mostly accounted for by surface-dwelling taxa like E. huxleyi, particularly in stations on the shelf and upper slope where the BP was well developed. The boundary between the BP and the underlying winter mixed layer was marked by a distinct step in T and S, clearly visible in all the CTD profiles, except those from the most offshore stations, where the plume is absent and the winter mixed layer occupies the entire water column up to the surface (stations 132 and 251).

Figure 2.8 - Vertical distribution of the more abundant coccolithophore taxa (> 2000 cells/l) in the upper 110 m of the water column during the 1st leg (light grey symbols) and 2nd leg (dark grey symbols). Boxes represent 1st, median and 3rd quartile of abundance distribution, whiskers represent minimum and maximum abundance. Samples from the turbid bottom nepheloid layer (BNL) were counted separately and represented in the grey band marked BNL. Note that Total, E. huxleyi and Total except E.h. are represented on an order of magnitude higher abundance scale than all other taxonomic groups.

68 Late winter coccolithophore bloom

Highest cell densities of E. huxleyi occurred west of Cape Carvoeiro, where it appeared closely associated with the highest Chl-a concentrations and maxima of small-chain diatom species considered to be 1st stage taxa in phytoplankton succession (Margalef, 1978) (e.g. Thalassiosira spp., Chaetoceros spp., Skeletonema spp.). The significant increase of G. oceanica and C. mediterranea during the 2nd leg appeared also closely related with the superficial BP. Maxima of G. oceanica occurred close to the coast west off Cape Carvoeiro (station 238), whereas the maximum of C. mediterranea was reached further offshore at the northern valley (station 146). In the latter area, modest increases in some other species such as Syracosphaera spp. and Ophiaster spp., were observed, as well as a broader vertical distribution of coccolithophores and stronger correlation between coccolithophore cells and phytoplankton biomass (Chl-a). This makes the northern valley appear different from the area off Cape Carvoeiro. A similar increase in abundance was not noticed in the most oceanward stations where the BP was absent and the winter mixed layer occupied the entire water column up to the surface (stations 132 and 251, respectively Figure 2.9c,f). In those stations, E. huxleyi was subordinate to less prolific surface dwellers like G. ericsonii and subsurface dwellers like Ophiaster spp. and Syracosphaera spp. even during the 2nd leg. The latter genera were observed displaying a broad vertical distribution along the entire 100 m at these distal locations.

2.4.5. Multivariate analysis

In order to explore and statistically demonstrate the rapid response of coccolithophore taxa (and phytoplankton s.l.) to the short-term environmental variations that occurred during the cruise, factor analysis was performed using the cell densities of the dominant coccolithophore taxa and the physical–biological proxies as variables in one single data matrix. In view of the very different environmental conditions and ecological responses encountered during the two legs of the cruise, factor analysis was performed on data from each of the two legs of the cruise separately. Only the samples for which nutrient data were available were considered as cases in the factor analysis. Since the lateral coast-to-ocean and vertical water column gradients appear as the most significant ecological gradients, factor scores were plotted against distance to coast and water depth (Figures 2.10–2.12). Four factors explained 55 % and 73 % of the total variance in the data from, respectively, the 1st and 2nd leg, of which Factor 1 (F1) and Factor 2 (F2) were considered the most statistically relevant for subsequent environmental analysis (Table 2.2). For the 1st leg, F1 (28 %) is mostly represented by nutrients (positive loadings) in opposition to salinity, temperature and Syracosphaera spp. (negative loadings), whereas F2 (13 %) is represented by Chl-a, Ophiaster spp. and Gephyrocapsa ericsonii (positive loadings).

Samples influenced by the factor assemblage NOx, PO4 and SiO2 (F1 positive scores) are better represented at the surface water level close to the coast (Figure 2.10a). The lack of nutrient data at the surface of the more distal stations (i.e. 122 and 131) limits our perception

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Figure 2.9 - Water column profiles of phytoplankton biomass (µg/l), temperature (°C), salinity (PSS-78), suspended particulate matter (FTU) and coccolithophore assemblages from three representative stations of the 1st leg of the cruise: Station 85 (306 m), Station 122 (1311 m) and Station 132 (3478 m), and three stations of the 2nd leg of the cruise: Station 236 (100 m), Station 146 (171 m) and Station 251 (1589 m).

Late winter coccolithophore bloom about its latitudinal distribution at surface level. Below the surface this assemblage is practically inexistent or weakly represented. Samples influenced by the factor assemblage salinity, temperature and Syracosphaera spp. (F1 negative scores) are mostly found at deeper levels below the surface and further offshore along the entire uppermost 100 m. Samples influenced by the factor assemblage Chl-a, Ophiaster spp. and G. ericsonii (F2 positive scores) are preferentially distributed further offshore, revealing a rather broad vertical distribution (Figure 2.10b). For the 2nd leg, F1 (38 %) is represented by temperature and salinity (positive loadings) in opposition to E. huxleyi, turbidity, Chl-a, G. oceanica, C. mediterranea, S. dalmaticus and H. carteri (negative loadings), whereas F2 (16%) is represented by G. muellerae, Syracosphaera spp. and G. ericsonii (positive loadings) in opposition to temperature (negative loadings). Samples influenced by the factor assemblage E. huxleyi, turbidity, Chl-a, G. oceanica, C. mediterranea, S. dalmaticus and H. carteri (F1 negative scores) are better represented at the surface water level in more neritic-coastal regions, i.e. off Cape Carvoeiro (Figure 2.11a) and at the northern valley (Figure 2.12a). Underneath the surface and further offshore along the entire water column, this assemblage appears nearly absent. Samples influenced by temperature and

Table 2.2 - Factor loadings (varimax raw), eigenvalues and percentage of the explained variance extracted from the data matrices referring the two legs of the cruise (r-mode Factor Analysis by Statistica 10; marked loadings are >0.6). Hc – Helicosphaera carteri, Go – Gephyrocapsa oceanica, Gm – Gephyrocapsa muellerae, Cm – Coronosphaera mediterranea, Syraco – Syracosphaera spp., Eh – Emiliania huxleyi, Ge – Gephyrocapsa ericsonii, Sdalm – Syracolithus dalmaticus, Ophi – Ophiaster spp., Arob – Algirosphaera robusta, T – Temperature, S – Salinity, Turb – Turbidity, Chl-a – phytoplankton biomass.

1st leg 2nd leg

F1 F2 F1 F2

Hc 0.0 0.0 -0.6 -0.1 Go -0.2 -0.2 -0.7 0.0 Gm 0.0 -0.4 0.3 0.8 Cm 0.2 0.5 -0.6 0.0 Syraco -0.6 0.2 0.3 0.8 Eh 0.4 0.0 -0.9 -0.2 -0.2 -0.2 Ge 0.6 0.8 Sdalm 0.5 -0.1 -0.6 -0.3

Ophi -0.4 0.6 0.2 0.5 Arob -0.2 0.2 0.1 0.1 T -0.9 0.1 0.7 -0.6 S -1.0 -0.1 0.7 0.1 Turb 0.3 -0.3 -0.9 0.0 Chl-a 0.3 0.8 -0.7 -0.1

NOx 0.9 0.0 0.4 0.0 PO 0.7 0.0 0.5 0.1 4 SiO2 0.6 0.0 -0.1 0.1

Eigenvalues 4.7 2.1 6.5 2.8

Total variance (%) 28 13 38 16

71 Chapter 2 salinity (F1 positive scores) are mostly related to a further offshore location (station 251), broadly distributed along the uppermost 50 m depth (Figure 2.12a). Samples influenced by the factor assemblage G. muellerae, Syracosphaera spp. and G. ericsonii (F2 positive scores) are mostly distributed further offshore, with the strongest signal recorded at the NW limit of the study area broadly distributed along the uppermost 50 m (station 251) and more weakly represented at the surface water layer of station 146, at the northern valley (station 146). Temperature (F2 negative scores) is weakly opposed to the former assemblage and generally better represented west of Cape Carvoeiro (Figure 2.11b). Results from factor analysis were generally statistically significant, particularly during the 2nd leg, when a clear response of phytoplankton in general, and coccolithophores in particular, to nutrient availability at the surface, was observed. The contrast between the two legs and the quick change of hydrographic conditions and related phytoplankton response is well represented by the lower versus higher statistical significance obtained for the 1st and 2nd legs, respectively. Lower percentage of explained variance obtained for the 1st leg reflects the more steady-state and low-productive ecological conditions during this period, when phytoplankton was not yet significantly developing, neither taking advantage from the nutrient-rich BP. Most of the physical and biological variables, including the most abundant coccolithophore taxa, revealed a distribution quite near the normal. Only the less abundant species are the most deviant from normal because their frequent zero abundance appears overvalued within the overall distribution (i.e. H. carteri, S. dalmaticus and A. robusta).

Figure 2.10 – Water column density section (kg/m3) for a transect along the axis of the upper and middle part of the Nazaré Canyon, with spatial distribution of scores from Factor 1 (a) and Factor 2 (b) obtained from the coccolithophore data from the 1st leg. For taxonomical references, see Table 2.2.

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Figure 2.11 – Water column density section (kg/m3) for a transect off Cape Figure 2.12 – Water column density section (kg/m3) for a transect along the Carvoeiro, with spatial distribution of scores from Factor 1 (a) and Factor 2 northern valley cutting the shelf-break north of Nazaré Canyon, with spatial (b) obtained from the coccolithophore data from the 2nd leg. For distribution of scores from Factor 1 (a) and Factor 2 (b) obtained from the nd taxonomical references, see Table 2.2. coccolithophore data from the 2 leg. For taxonomical references, see Table 2.2.

Chapter 2

2.5. Discussion

2.5.1. Buoyant plume dynamics during a late winter upwelling event

The reported hydrographic profiling and plankton sampling coincided with a period of transient oceanographic and meteorological conditions, characteristic for the late winter period. Relatively warm and saline oceanic waters fed by the IPC were present in the winter mixed layer which occupied the upper 100–200 m of the water column over the shelf and upper slope, as typical during winter (e.g. Oliveira et al., 2004). A superficial layer of relatively cool and low saline water capping the warmer and more saline winter mixed layer water was noticed during both legs of the cruise. This buoyant plume was presumably fed by runoff from intense rainfall that occurred prior to and at the beginning of the cruise. Fresh water was possibly originating from rivers north of the study area (e.g. Lis, Mondego, Douro rivers) as well as from small rivers flowing directly into the Nazaré Canyon head (e.g. Alcôa, Tornada and Arnoia rivers) (see Figure 2.1). Lowest salinities in the superficial layer, and strongest vertical gradients were recorded during the 1st leg, along the upper Nazaré Canyon. Equatorward and offshore extension of the BP most probably occurred as a consequence of Ekman superficial dynamics driven by the prevailing northerly winds. As lighter waters were continuously being advected above the denser winter mixed layer, vertical stratification of the Ekman layer increased and the seaward side of the BP was stretched. Nearer to the coast, the greater thickness of the BP suggests that it was subject to mixing at its base with the underlying denser waters which were brought up from deeper levels by the Ekman circulation. Whilst mixing was levelling off the vertical density gradient at the base of the plume along its coastal side, the BP continued to move in offshore direction until it eventually got separated from the coast (see Fong and Geyer, 2001; Santos et al., 2004). Similar cases where local winds control the dynamics of river plumes and coastal upwelling have been described by several authors. Fong and Geyer (2001) argue that a moderate-amplitude upwelling wind lasting a few days induces significant mixing in the plume, advecting and spreading it far off the coast, whereas under sustained upwelling winds the plume is gradually spread out to nearly uniform thickness. Such has already been described from off the Portuguese coast during occasional winter upwelling events, when Ekman surface circulation was observed to advect the plume to more than 100 km offshore in a few days (Otero et al., 2008). Convergence of the BP with the IPC was reported to occur at the shelf break, leading to local thickening of the plume, favouring the retention of biological material in this area (Peliz and Fiúza, 1999; Santos et al., 2004; Ribeiro et al., 2005). Such a scenario appears to apply also to our cruise: whereas river runoff decreased, the northerly wind-driven Ekman circulation persisted, causing the BP to spread further offshore and become detached from the coast. Nevertheless, contrary to summer upwelling episodes, during which northerly winds are more intense and persistent over the Portuguese coast (e.g. Peliz et al., 2002; Alvarez-Salgado et al., 2003), the observed northerly wind event was probably not persistent enough to bring nutrients from below the deep (~150 m) seasonal

74 Late winter coccolithophore bloom pycnocline (e.g. Ribeiro et al., 2005). Moreover, vertical profiles along the uppermost 1000 m of stations from the 1st leg (data not shown) revealed that nutrient concentrations significantly decreased from the surface down to 250 m depth and thus, no significant input would be expected from the levels immediately below the pycnocline. Therefore, the observed upwelling event should be viewed in terms of its capacity to spread a thin nutrient-rich BP from the coast towards offshore, rather than as a mechanism of nutrient replenishment from subsurface waters. That highest nutrient concentrations were measured within the BP indicates that nutrients were being sourced mainly by runoff discharged by rivers prior to and at the beginning of the cruise. In comparison to some other areas of the world’s oceans, nutrient concentrations during the cruise can be considered as generally low (Levitus et al., 1993), but enough to support the phytoplankton communities thriving in this area (see Section 2.4.2). N:P ratios falling below the typical 16:1 Redfield ratio in surface waters during the 2nd leg point at nitrogen as the main limiting nutrient for phytoplankton growth, in good agreement with several studies within coastal waters (Redfield, 1958; Redfield et al., 1963; Ryther and Dunstan, 1971; Fisher et al., 1992; Labry et al., 2002; Mendes et al., 2011).

2.5.2. Productivity variations on a weekly basis

Results presented in this study strikingly illustrate the rapid response of phytoplankton to favourable environmental conditions. A brief period of northerly winds was enough to promote spreading of the nutrient-rich BP, favouring a massive increase in phytoplankton biomass and coccolithophore cell densities from the 1st to the 2nd leg of the cruise. Vertical stratification associated with the BP appears to have acted as a mechanism retaining both nutrients and cells within the sunlit surface layer, leading to a remarkable phytoplankton bloom in the otherwise relatively nutrient-poor oceanic conditions that prevail during winter on the central Portuguese margin (see Santos et al., 2004; Ribeiro et al., 2005). Cells and nutrients were clearly associated with the salinity minima of the BP and were probably advected along with it. This would explain why the highest concentrations of Chl-a and coccolithophore cells occurred preferentially at the surface of the more distal part of the transect west off Cape Carvoeiro, where the BP was thinner and more sharply defined at the surface. A map of Chl-a average concentration for March 2010 obtained from satellite data (see Figure B in Auxiliary Material) illustrates the broad spreading of this Chl-a enrichment, extending from the coast to the middle shelf region, and apparently originating from the north. Although nutrients were already available at the time of the 1st leg of the cruise, and probably were still being replenished by runoff from land, a clear response in phytoplankton productivity was only observed during the 2nd leg. Such delay may be explained partly by the higher advective mixing between the BP and shelf's ambient waters and significant cloud coverage during the 1st leg (see Figure 2.2). When river runoff had decreased at the end of the 1st leg, the intensity of mixing between the BP and the denser water layer below probably weakened, leading to stabilization of the vertical stratification (see Ribeiro et al., 2005). The

75

Chapter 2 retention of cells within the BP promoted exposure of phytoplankton to sunlight and allowed cell division to remain constant as long as the cells remained inside the BP (e.g. Smetacek and Passow, 1990; Ribeiro et al., 2005). With nutrient availability ensured within the BP, light seems logically the ultimate factor needed to set off the phytoplankton bloom. Clear skies and slight increase of PAR (see Figure 2.2) occurring in the interval between the two legs of the cruise may have provided the required favourable light conditions. Another factor that possibly contributed to the establishment of favourable conditions for phytoplankton to bloom within the surface layer was the relatively low suspended sediment load in the BP, therefore not significantly reducing light availability. River floods occurring in autumn and early winter, when river basins are still loaded with accumulated fine sediments, tend to discharge much more turbid waters onto the shelf, thereby inhibiting phytoplankton growth. Waters discharged as a result of the late winter flood prior to our cruise were probably relatively clear. The moderate sea wave conditions also contributed to the generally low turbidity values during the cruise, and to the persistence of the water stratification, long enough to allow the development of a phytoplankton bloom at the surface. Even so, settling of suspended sediment from the BP as it spread out in offshore direction may have played a role in improving light conditions near the surface as well as in deeper water. Change from a suspension-related turbidity during the 1st leg, to phytoplankton-related turbidity during the 2nd leg supports this hypothesis (see Figure A in Auxiliary Material). Wind-driven turbulence, water stratification and mixed-layer depth were already demonstrated to be important factors controlling phytoplankton access to its basic requirements for growth: light and nutrients (Doyon et al., 2000; Kudela et al., 2005). The importance of river runoff in providing nutrients to phytoplankton communities, and stratification of the upper water column as a key-factor in the occurrence of phytoplankton blooms during winter and spring on the Portuguese continental shelf, have also been confirmed by several authors (Peliz and Fiúza, 1999; Moita, 2001; Varela et al., 2001; Ribeiro et al., 2005; De Castro et al., 2006). Moita (2001) found that Chl-a peaks during winter were associated with runoff-driven haline-stratification, particularly north of Cape Carvoeiro, and that phytoplankton growth during spring occurred at the expense of nutrients replenished during winter when thermal stratification was still weakly developed. During this transient period the relatively well-mixed water column showed a certain degree of stability at the uppermost water levels, where blooms occurred very close to the surface following calm and relatively warm days and in the presence of some haline-stratification. Peliz and Fiúza (1999), analysing Coastal Zone Colour Scanner images obtained between 1979 and 1985, concluded that the highest Chl-a concentrations occurred in winter over the shelf and slope, extending to large distances off the coast. They appeared associated with the offshore spreading of river plumes, eventually occupying the whole shelf and slope zone in about one week (e.g. Peliz and Fiúza, 1999; Santos et al., 2004). The role of Cape Carvoeiro in rapidly redirecting the nutrient-rich BP further offshore, following similar dynamics as associated with the generation of chlorophyll-rich upwelling filaments extending to the ocean during summer, should not be discarded (e.g. Fiúza, 1983; Haynes et al., 1993; Peliz et al., 2002).

76 Late winter coccolithophore bloom

The late winter bloom here described occurred at the expense of nutrients within the BP, as indicated by the significant decrease of NOx, PO4 and SiO2 at the surface. A lesser decrease in nutrient concentrations at deeper levels is indicative of lower consumption rates below the surface (Figure 2.4). Chl-a concentrations reported in this study revealed to be much higher than so far reported from the Portuguese margin, with a maximum Chl-a of 13 mg/l off Cape Carvoeiro, compared to 4.3 mg/l in the Nazaré canyon region in June of 2006 (Mendes et al., 2011), max. 4.6 mg/l off Cape S. Vicente and along the coastal region north of Cape Carvoeiro, during summer, and max. 6.3 mg/l off Faro, during spring (Moita, 2001), max. ~3.5 mg/l in the NW region of the Portuguese shelf, February of 2000 (Ribeiro et al., 2005), and max. 5.3 mg/l in Lisbon Bay, February 2005 (Silva et al., 2009). The winter–spring transition may thus lead to a stronger ecological response than occurring during the summer-upwelling season, when wind and sunlight conditions are usually more persistently favourable. Pigment data from this period indicate that diatoms were the dominant phytoplankton group and the main contributor for Chl-a production, particularly at the uppermost water layer

(data not shown). The conspicuous depletion of SiO2 at the surface, observed especially off Cape Carvoeiro therefore likely reflects the bloom of small-chain diatoms (see Margalef, 1978).

Rapid exhaustion of silica by diatoms apparently led coccolithophores to profit from NOx and

PO4 still available at the surface, contributing to their unexpectedly rapid and significant bloom near the coast.

2.5.3. Coccolithophore ecological preferences

Often considered as a uniform functional group of calcifying phytoplankton thriving in low-turbulence, low-nutrients and high-light environments, results presented in this study clearly show that coccolithophore life strategies are much more diverse than expected. The most striking ecological variations occurred along the coastal-oceanic lateral gradient and vertically along the upper photic layer. It is clear that some taxa were favoured by the offshore spread of the BP, taking profit from nutrient and light availability at the surface, whereas others preferably developed below the surface and further offshore, away from the influence of river runoff (see Figures 2.9–2.12). Results from factor analysis clearly confirmed such short-term ecological changes. Factor analysis for the 1st leg clearly illustrates the strongest contrast between the coastal- neritic region affected by nutrient rich runoff waters in the BP and the oceanic mixed water mass further offshore observed in this period. Only few coccolithophore species displayed some direct relation with such lateral gradient: subsurface dweller Syracosphaera spp. preferably associated to more oceanic and oligotrophic water conditions below the surface and along the entire uppermost 100 m further offshore (F1, Figure 2.10a), whereas Ophiaster spp., G. ericsonii and, to a lesser extent, C. mediterranea, were more associated to (low) phytoplankton productivity (Biom Chl-a) occurring at the surface closer to the coast (F2, Figure 2.10b).

77

Chapter 2

The observed coccolithophore bloom at the expense of nutrients within the BP is clearly showed by factor analysis performed for the 2nd leg. E. huxleyi, G. oceanica and C. mediterranea were the more productive and contributor species for the remarkable increase of Chl-a observed in this period (F1, Figures 2.11 and 2.12a), whereas G. muellerae, Syracosphaera spp., G. ericsonii and Ophiaster spp. were more independent from the nutrient- rich BP and preferentially developing offshore, outside the influence of runoff (F2, Figure 2.12b). The observed dominance of E. huxleyi during both low- and high productivity periods during the cruise is in good agreement with its presumed cosmopolitan and opportunistic behaviour (Winter et al., 1994; Baumann et al., 2000; Andruleit, 2007; Boeckel and Baumann, 2008). The remarkable occurrence of E. huxleyi together with small-chain diatoms and significantly contributing to phytoplankton biomass during the high productive period, supports earlier observations identifying it as an early succession r-selected species, capable of rapid growth within nutrient-rich, turbulent environments (e.g. Giraudeau and Bayley, 1995; Andruleit and Rogalla, 2002; Sprengel et al., 2002; Andruleit, 2007; Silva et al., 2008) and constituting the main bloom-forming coccolithophore (e.g. Okada and Honjo, 1973; Knappertsbusch and Brummer, 1995; Garcia et al., 2011; Souza et al. 2011). G. oceanica was apparently “dormant” during the low-productive period (1st leg) but rapidly developed as soon as nutrient-light stratification conditions became favourable during the 2nd leg. It manifests itself as one of the species better adapted to thrive within nutrient-rich, competitive conditions near the coast, although not reaching cell densities as high as those of E. huxleyi. Results agree with several authors referring to it as a typical coastal coccolithophore, well adapted to the nutrient-rich and productive environment off Portugal (Silva et al., 2008), and as maximum upwelling indicator, based on its quick response to nutrient input (Winter et al., 1994; Giraudeau and Bayley, 1995; Broerse et al., 2000; Andruleit and Rogalla, 2002; Sprengel et al., 2002; Andruleit et al., 2003). C. mediterranea was also able to profit from nutrient favourable conditions during the cruise and flourished in the 2nd leg, although less prominently than the two latter, and more displaced towards the shelf-break region, at the northern valley. Silva et al. (2008) and Moita et al. (2010) also reported the presence of high cell densities of C. mediterranea off the Nazaré region during winter, referring to it as a good tracer for the convergence of subtropical waters (ENACWst) onto the Portuguese shelf during the upwelling-downwelling transition. Despite the generally low abundance of S. dalmaticus, correlation of this species with E. huxleyi, G. oceanica and C. mediterranea, closer to the coast off Cape Carvoeiro, suggest that it has some capacity to profit from nutrient availability, in the context of moderate-to-low turbulence within coastal regions. This contradicts previous studies which associate holococcolithophores with more oligotrophic and oceanic environments (i.e. Mediterranean Sea, NE Atlantic, Red Sea and Gulf of Aden, Kleijne, 1991). Observations on Syracosphaera spp. are consistent with Andruleit (2007) in terms of its broad depth range but contradict several studies reporting this genus as having affinity for nutrient availability in coastal regions (e.g. Andruleit and Rogalla, 2002; Andruleit, 2007). In

78 Late winter coccolithophore bloom addition, little is known about S. marginoporata, the dominant species within this group (max. 1.4×104 cells/l counted with SEM). The same applies to Ophiaster spp. which, similarly to Syracosphaera spp., includes a variety of species which cannot be distinguished with PLM but which are expected to have distinct ecological preferences (Young, 1994). Lack of taxonomical differentiation and of a systematic quantification of typical nutrient levels in the above- mentioned studies may partially explain discrepancies with the present study. G. ericsonii was the second most abundant species during the cruise, next to E. huxleyi, confirming its preference for nutrient enriched coastal/neritic regions inferred by several authors (e.g. California Current System, Winter et al., 1979; south of Benguela upwelling system, Giraudeau and Bayley, 1995; Lisbon Bay, Silva et al., 2008). Yet, its highest cell densities further offshore during the high productivity period, away from the influence of the BP and coastal turbulence, suggest that it is better adapted to compete with E. huxleyi in oceanic conditions than in coastal waters. Although with much lower abundances, G. muellerae displayed an ecological performance similar to G. ericsonii: higher abundances and coastal- neritic distribution during the 1st leg and better performance in more oceanic regions during the high-productive period, suggesting it has a more oligotrophic behaviour on the central Portuguese margin, in comparison to other placolith-bearing species (i.e. G. oceanica and E. huxleyi). The two species are apparently able to thrive and dominate the coccolithophore community under steady-state low-productive conditions over the shelf, but not when shelf and coastal waters become favourable for r-selected species like E. huxleyi and G. oceanica. The observed higher diversity of coccolithophore species, broader vertical distribution and stronger correlation between cells and phytoplankton biomass (Chl-a) at the shelf-break region (northern valley), possibly reflect the dominance of this group within more distal regions.

2.6. Conclusions

Coccolithophores off central Portugal showed a rapid response to regional meteorological and hydrographic variations occurring in late winter between 9 and 19 March 2010, either taking profit of nutrient availability in coastal-neritic areas and competing with other r-selected phytoplankton groups (e.g. small-chain diatoms), or preferentially developing in more oceanic- oligotrophic regions, where competition with r-selected taxa is expectedly lower. Over the relatively warm and saline winter mixed layer water occupying the upper 100– 200 m of the water column over the shelf and upper slope, a superficial nutrient-rich Buoyant Plume (BP) of relatively cool and low-saline water, presumably fed by runoff from intense rainfall that occurred prior to and at the beginning of the cruise, was spread out equatorwards and offshore, most probably as a consequence of Ekman superficial dynamics generated by the prevailing northerly winds. Whereas river runoff decreased, the Ekman circulation driven by the northerly wind made the BP to spread further offshore and become detached from the coast. Despite relatively high nutrient availability within the BP, cloud cover and initial relatively high

79

Chapter 2 turbidity within the BP resulted in sub-optimal light conditions unfavourable for the growth of phytoplankton (Figure 2.13a). In the transition towards the 2nd leg, stable density stratification, decreasing turbidity at the surface and prevailing clear skies finally allowed phytoplankton to take advantage of the nutrients retained in the BP. In the shelf and upper slope area covered by the BP, E. huxleyi and G. oceanica were the coccolithophore species that benefited the most from favourable nutrient conditions within the sunlit layer. C. mediterranea and S. dalmaticus also responded to the favourable conditions, although less notably than the first two species (Figure 2.13b).

Figure 2.13 – Schematic representation of the environmental conditions that contributed to the late winter coccolithophore bloom observed during the cruise: (a) 1st leg, low-productive pre-bloom period: the wind regime was shifting from southerlies to northerlies, and the vertical gradient between the BP and the winter mixed layer was strongest due to still significant river discharge; (b) period between legs: clear sky conditions were most favorable, runoff driven turbidity at the surface had decreased, and northerly wind forced Ekman circulation of the BP was strongest, all factors contributing to trigger the phytoplankton and coccolithophore bloom in the BP; (c) 2nd leg, high-productive bloom period: significant Chl-a and cell concentrations were recording a bloom at the surface, at the expense of nutrient provided by the plume, with E. huxleyi, G. oceanica and C. mediterranea revealing a remarkable increase of abundance between the coast and the shelf-break. During this time, the BP was relatively more mixed with the underneath winter layer, the wind regime changed back to southerlies and an increase of cloud coverage was noticed (C. mediterranea – Cm; E. huxleyi – Eh; G. ericsonii – Ge; G. muellerae – Gm; G. oceanica – Go; Ophiaster spp. - Ophi; Syraco. dalmaticus – Sdalm; S. marginoporata – SM; Buoyant Plume – BP).

80 Late winter coccolithophore bloom

Syracosphaera spp. and Ophiaster spp. were the most consistently oligotrophic taxa, constituting an important component in offshore assemblages and displaying a broad vertical distribution extending well below the nutrient-rich surface layer in the more coastal-neritic regions. G. ericsonii and G. muellerae decreased in abundance in shelf and upper slope waters, but increased in the most offshore waters where E. huxleyi was not significantly developing (Figure 2.13a). The observed rapid response of coccolithophores to short-term meteorological and hydrographic variability presents a challenge to the application of coccoliths in paleoclimatic and paleoceanographic reconstructions, and demonstrates the need for improved knowledge of the ecological characteristics of this group.

Acknowledgements - This research was supported by the HERMIONE project (EC contract 226354) funded by the European Commission and the Cd Tox-CoN project (FCT-PTDC/MAR/102800/2008) funded by the Portuguese Science Foundation FCT. The first author benefits from an FCT PhD grant (FRH/BD/41330/2007). The authors are grateful to the crew of the NRP Almirante Gago Coutinho and several researchers participating in the 2nd HERMIONE cruise conducted by IH for their valuable help during the collection of samples. All the samples were prepared and analyzed in NANOLAB, Geology Centre of Lisbon University (CEGUL). SEM observations were made at the Institut de Ciències del Mar (ICM—CSIC, Barcelona, Spain). We also thank João Vitorino and Inês Martins (IH, Oceanography Dep.) for compiling CTD data, Manuela Valença (IH, Chemistry and Pollution Dep.) for analyzing and compiling nutrient data, and Francisco Silva and Sara Almeida (IH Oceanography Dep.) for providing wave and wind data. Constructive criticism and helpful suggestions from two anonymous reviewers are most gratefully acknowledged by the authors.

81

Auxiliary Material

Figure A - Scatter plots of water turbidity (FTU) versus phytoplankton biomass (Chl-a, µg/l) measured during the 1st and 2nd leg of the cruise, showing no correlation during the 1st leg (a), changing to a strong positive correlation during the 2nd leg (b).

Figure B - Regional maps obtained from satellite data, representing the monthly averaged Chl-a production in the Nazaré Canyon region during (a) February, (b) March and (c) April of 2010.

Chapter 3

Influence of the Nazaré Canyon, central Portuguese margin, on late winter coccolithophore assemblages

Chapter 3 Influence of the Nazaré Canyon, central Portuguese margin, on late winter coccolithophore assemblages

Re-submitted as: C. Guerreiro, C. Sá., H. de Stigter, A. Oliveira, M. Cachão, L. Cros, C. Borges, L. Quaresma, A.I. Santos, J.-M. Fortuño, A. Rodrigues,. Influence of the Nazaré Canyon, central Portuguese margin, on late winter coccolithophore assemblages. Deep-Sea Research, Special Issue – Submarine canyons.

Abstract

This paper presents a first attempt to characterize coccolithophore assemblages occurring in the context of an active submarine canyon. Coccolithophores from the upper-middle sections of the Nazaré Canyon (central Portuguese margin) - one of the largest canyons of the European continental margin - were investigated during a late winter period (9 – 12 March 2010). Species distributions were analyzed in a multiparameter environmental context (temperature, salinity, turbidity, Chl-a and nutrient concentrations). Monthly averaged surface water Chl-a concentration between 2006 and 2011 assessed from satellite data is also presented, as a framework for interpreting spatial and temporal distribution of phytoplankton in the Nazaré Canyon. The Nazaré Canyon was observed to act as a conduit for advection of relatively nutrient- poor oceanic waters of ENACWst origin into nearshore areas of the continental shelf (less than 10 km off the coast), whilst at the surface a nutrient-rich buoyant plume resulting from intensive coastal runoff prior and during the beginning of the cruise was spreading in oceanward direction. Two distinct coccolithophore assemblages appear representative for the coast to open ocean gradient: (1) Emiliania huxleyi together with Gephyrocapsa ericsonii and Coronosphaera mediterranea dominated the more productive assemblage present within coastal-neritic surface waters; and (2) Syracosphaera spp. and Ophiaster spp. displayed a higher affinity with open- ocean conditions, and also generally a broader vertical distribution. Local “hotspots” of coccolithophore and phytoplankton biomass potentially associated with perturbations of surface water circulation by the canyon are discussed.

Keywords: Living coccolithophores; Chl-a; ENACWst; submarine canyon

85 Chapter 3

3.1. Introduction

Submarine canyons incising the continental margins are prominent topographic features that modify the coastal circulation. By intensifying shelf-slope exchange of water and organic/inorganic matter they play a key-role in global biogeochemical cycling (e.g. Durrieu de Madron, 1994; Gardner, 1989; Hickey et al., 1986; Monaco et al., 1999; Puig et al., 2003). Narrow canyons tend to have a stronger effect on low-frequency circulation, whereas wider canyons mainly cause bottom flow adjustment along isobaths (Klinck, 1988). Stratification of the water column reduces the canyon’s topographic effect on the coastal flow (Hickey, 1997; She and Klinck, 2000). In the upper water layers (above 100 m), the influence of the canyon is only gentle, with the along-shelf flow turning slightly onshore upstream of the canyon and turning offshore downstream. Closer to the canyon rims (100-200 m) the along-shelf flow is more strongly deflected in onshore direction, turning back on the downstream side of the canyon, with upwelling or downwelling occurring above the rims, depending on the wind direction (She and Klinck, 2000). In the Northern Hemisphere right-bounded flows (i.e. coast to the right, looking downstream) induce downwelling conditions within the canyon, whereas left-bounded flows favor the occurrence of upwelling (Klinck, 1996; She and Klinck, 2000). Upwelling occurs mostly at the canyon head and downstream rim and adjacent shelf (Allen, 1996; Klinck, 1996; Mendes et al., 2011; She and Klinck, 2000). Under downwelling conditions, the canyon acts as a trap for converging shelf water (Skliris and Djenidi, 2006). The intensification of both coast to ocean and vertical water transport within submarine canyons is expected to affect the dynamics of plankton ecosystems in the vicinity of canyons (see Bosley et al., 2004; Hickey, 1995; Kampf, 2006; Ryan et al., 2005; 2010; Skliris et al., 2002; Skliris and Djenidi, 2006). Indeed a strong response of phytoplankton production to canyon flows, and concentration of marine organisms by physical processes within and around canyons were reported from several studies (e.g. Bosley et al. 2004; Macquart-Moulin and Patriti, 1996; Skliris and Djenidi, 2006). The Nazaré Canyon, located at the central Portuguese margin and one of the largest submarine canyons of Europe, has been relatively intensely explored with regards to its geology, geomorphology, oceanography and benthic biology (e.g. Tyler et al., 2009). Little is known, however, about the plankton communities thriving in this region, and about the canyon’s effect on their ecology. Guerreiro et al. (submitted-b) (Chapter 4) observed a relatively higher diversity of coccolith species, including both oceanic and coastal-neritic taxa but with a relative dominance of the latter, in the Nazaré Canyon in comparison to the adjacent shelf/slope regions. This was interpreted as reflecting the exchange of water masses between coastal and oceanic regions through the canyon, as well as the dynamic and nutrient-rich conditions where the coastal species are better adapted to survive. Locally enhanced productivity in the surroundings of the canyon may be related to persistent physical phenomena associated with the canyon such as vertical mixing by solitary internal waves (Quaresma et al. 2007), and/or upwelling in the

86 Influence of the Nazaré Canyon canyon head (Guerreiro et al., 2009). Evidence for local enhancement of phytoplankton productivity is also provided by observations on phytoplankton pigments reported by Mendes et al. (2011), with maximum values of Chl-a (indicative of phytoplankton in general) near the canyon head and maximum values of 19’ hexanoyloxyfucoxantine pigment (indicative of coccolithophores) found in the area north of the canyon. Here we report the results obtained from a plankton survey on living coccolithophores from the upper-middle Nazaré Canyon, during late winter (9 – 12 March 2010) (Figure 3.1). On the basis of a detailed characterization of the coccolithophore assemblages together with a general characterization of environmental conditions prevailing during the sampling period, the impact of this major submarine canyon on coccolithophores and phytoplankton biomass is discussed.

3.2. Regional setting

3.2.1. Oceanography

The central Portuguese continental margin is characterized by a relatively narrow shelf of a few tens of km width, with a maximum of ~70 km where it projects oceanward in the Estremadura promontory, but cut back to very close to shore where it is incised by the Nazaré and Lisbon-Setúbal Canyons. The Douro and Tagus are the most important rivers debouching on the shelf, with relatively minor contribution of continental runoff from other rivers. From the shelf edge located at 160-200 m, a steep upper slope and more gently inclined lower slope incised by numerous gullies and canyons, lead down to the Iberia and Tagus abyssal plains. Surface water circulation along the Portuguese margin is directly dependent on two main current systems transporting water eastwards across the North Atlantic: the North Atlantic Current extending to the north of the Iberian Peninsula, and the Azores Current south of Iberia (Barton, 2001; Peliz et al., 2005; Pollard and Pu, 1985; Saunders, 1982). As the Azores Current extends eastwards, branches of this current loop smoothly into the Portugal Current and further south into the Canary Current. The Portugal Current slowly flows southwards, west of Portugal, carrying about 2×106 m3/s in the upper 200 m of the water column. It partially continues further south into the Canary Current, while another part apparently enters the Mediterranean within a shallow surface layer (Barton, 2001; Saunders, 1982). The upper 500 m of water column off Portugal, including the surface mixed layer and the first thermocline, is constituted by the Eastern North Atlantic Central Water (ENACW). This water mass, representing the main source of the nutrient-rich upwelled waters on the Portuguese coast, shows considerable variation in its hydrological features as it travels along the coast (Fiúza, 1984; McCave and Hall, 2002). The ENACW has two main components of different origin that converge to this region: a lighter, relatively warm and salty subtropical branch (ENACWst) formed along the Azores Front, which gradually loses its characteristics as it travels further northwards along the Iberian margin; a less saline colder water mass of subpolar

87 Chapter 3 origin (ENACWsp) slowly flowing southwards below the poleward subtropical branch, related with the Subpolar Mode Water formed in the eastern North Atlantic by winter cooling and deep convection (Fiúza et al., 1998). Beneath the near-surface equatorward flow of the Portugal and Canary currents, the Iberian Poleward Current (IPC) can be recognized traveling poleward, counter to the general circulation and closely bound to the continental slope, its core extending about 300-400 m vertically. This current is mostly restricted to the subsurface layers along most of the eastern subtropical gyre, but surfaces whenever the Trade Winds weaken or turn northward (Barton, 2001). Circulation along the Portuguese shelf and upper slope is markedly seasonal, associated to the annual cycle of two major atmospheric systems: the Azores high and Iceland low pressure system, respectively (e.g. Barton, 2001; Haynes et al., 1993; Relvas et al., 2007). During summer, the Azores high pressure system migrates towards the central Atlantic, typically inducing Trade Winds to become northerly, inducing an equatorward circulation over the upper 150-200 m of the water column off Portugal. During winter, when the Azores high pressure system is located further south and the Iceland low pressure system intensifies, the dominant wind regime becomes southerly along the western Portuguese margin. This induces shoaling of the IPC over the upper slope and shelf, where the poleward flow produces an onshore Ekman transport, in turn resulting in downwelling conditions over the shelf (Fiúza, 1983; Vitorino et al., 2002). River runoff is an important feature of the winter circulation over the western Portuguese margin, through which a significant discharge of low salinity water occurs into the coastal ocean. This results in buoyant plumes that either develop into inshore currents (Relvas et al., 2007; Otero et al., 2008) or expand further offshore, under the influence of, respectively, southerly or northerly-winds over the shelf and slope (Otero et al., 2008). The Western Iberian Buoyant Plume, characterized by low salinity (<35.8) and low temperature compared to normal shelf waters, is mostly fed by outflow from rivers of northen Portugal (Mondego, Douro, Minho, Lima, Vouga). Besides these major rivers, other smaller rivers and lagoons contribute as well. Interannual variability of circulation along the Portuguese shelf and slope is influenced by the North Atlantic Oscillation (NAO), resulting from fluctuations in the difference of atmospheric pressure between the Azores high and the Iceland low. NAO high index conditions typically are associated with an increase of the trade winds that bring moist air into Europe, resulting in cool summers and mild and wet winters in Europe and its Atlantic forefront. On the contrary, NAO low index conditions leads to more extreme atmospheric temperatures, producing heat-waves and deep freezing, and an increase of storm activity and rainfall in southern Europe and North Africa. Several studies have indicated a decreasing intensity and increasing frequency in upwelling events, occurring even during the winter period (e.g. Alvarez et al., 2009; Barton, 2001; Ribeiro et al., 2005; Santos et al., 2004; Silva et al., 2008; Vitorino et al., 2002), apparently linked with a trend towards the “high index” mode of the NAO observed over the last decades, leading also to mild, wet winters over northern Europe and dry conditions

88 Influence of the Nazaré Canyon over Portugal (Barton, 2001; Wallace, 2002). In addition to thermohaline and wind-driven circulation, tidal currents are also important in influencing the hydrodynamics of the Portuguese margin. Particularly where the M2 semi- diurnal tidal current, the dominant tidal constituent over the Portuguese margin, forces stratified upper ocean water over the abrupt topography of the slope and shelf-break (e.g. Quaresma and Pichon, 2011), tidal energy is transferred into baroclinic motions in the form of internal waves and internal tides. These are very important in mixing the ocean water column, enhancing vertical nutrient transport and thus phytoplankton productivity (e.g. Guerreiro et al., 2009), as well as in increasing bottom turbulence over the continental shelf and slope, triggering bottom sediment resuspension and transport (Huthnance et al., 2002). “Hotspots” of internal tide generation on the Portuguese margin appear associated with submarine canyons cutting across the shelf and slope (e.g. Portimão canyon, Bruno et al., 2006; Nazaré Canyon, Quaresma et al., 2007; Quaresma and Pichon, 2011) and with promontories of the continental shelf (e.g. Estremadura spur, Quaresma and Pichon, 2011).

3.2.2. Nazaré Canyon

The Nazaré Canyon, the largest submarine canyon of the Portuguese margin, cuts completely across the shelf and slope, from less than 1 km from the coastline off the village of Nazaré at a water depth of about 50 m to a distance of >210 km from the coast and a water depth of 5000 m. An upper, middle and lower section can be distinguished on the basis of general morphology and characteristics of the hydrodynamic and sedimentary environment (Vanney and Mougenot, 1990; De Stigter et al., 2007; Lastras et al., 2009). The upper canyon section consists of a narrow and distinctly V-shaped meandering valley that lies deeply entrenched in the shelf. Beyond the shelf edge, it passes into the much broader and U-shaped middle section incised in the continental slope. The lower canyon section consists of a broad and flat-floored valley at the base of the slope, opening at 5000 m water depth into the Iberia Abyssal Plain. The physical oceanography of the Nazaré Canyon has been summarised by Tyler et al. (2009), largely on the basis of CTD and current meter data collected by the Portuguese Hydrographic Institute and Royal NIOZ (final reports of the EUROSTRATAFORM, HERMES and HERMIONE European projects). Inside the Nazaré Canyon, residual currents are generally aligned along the canyon axis as the result of strong topographical control. The current alignment extends well above the canyon edges (~150 m depth) implying substantial disturbance of the predominant north-south circulation parallel to the general trend of the shelf and slope. At depths shallower than 300 m, the residual currents inside the canyon show a distinct coupling to the wind-driven current regime over the continental shelf. During winter, the occurrence of downwelling conditions over the shelf results in a down-canyon residual flow near or just above the canyon edge. Under strong upwelling conditions and southward flow

89 Chapter 3 across the shelf, onshore (up-canyon) flow is observed in the upper canyon, with intensification of upwelling near the canyon head. The enhancement of upwelling and associated bottom resuspension can be expected to provide a nutrient source supporting enhanced phytoplankton concentration south of the canyon (e.g. Hickey, 1995; Kampf, 2006). This seems to be confirmed by observations by Mendes et al. (2011) regarding phytopigment distribution patterns in surficial waters around the Nazaré Canyon, with maximum concentrations of diatoms occurring south of the canyon. The interaction of the external (barotropic) tide off the Portuguese coast with the canyon topography, in the presence of water stratification, leads to the generation of internal (baroclinic) tides (i.e. internal waves of tidal period), which radiate from the generation point and propagate the tidal energy vertically (Quaresma et al., 2007; Tyler et al., 2009). Strong semi-diurnal bottom currents occur in all parts of the canyon, particularly in its upper and middle sections (commonly exceeding 30 cm/s) which, along with the ample supply of fine- grained sediments from the shelf, result in the permanent haze of suspended matter in the upper canyon (De Stigter et al., 2007). The generation of non-linear internal waves (NIW) at the canyon’s northern shelf break and their refraction towards NE was observed by Quaresma et al. (2007) mainly during summer, when stratification of the shelf waters supports the waves. Observations indicate that the NIW most likely result from the interaction of the semidiurnal M2 barotropic tide with the canyon rim, displaying horizontal and vertical velocities strong enough to resuspend bottom sediments along the wave propagation path from the middle to the inner shelf. The injection of nutrients from the lower toward the upper levels of the water column forced by the shoreward propagation of these NIW has been invoked to explain high concentrations of coccoliths found in the sedimentary cover in this near shore position (Guerreiro et al., 2009). Although this mechanism occurs mainly during spring and summer, it seems persistent enough to explain such anomaly in coccolith distribution. In autumn and winter, violent westerly storms generating waves with significant height up to 9 m cause widespread sediment resuspension on the shelf and downwelling of turbid waters towards the canyon. The location of the canyon head at less than 1 km from the shore makes it particularly prone to trap particulate matter transported as bedload and in suspension along the shelf (De Stigter et al., 2007; Oliveira et al., 2007).

90 Influence of the Nazaré Canyon

3.3. Material and methods

3.3.1. Sample collection

Sampling was conducted between 9 and 12 of March 2010, on board of NRP “Almirante Gago Coutinho” during the 2nd HERMIONE (Hotspot Ecosystem Research and Man’s Impact On European Seas) scientific cruise of the Portuguese Hydrographic Institute. Coccolithophore communities were investigated in 97 water column samples collected at discrete water depth levels between 5 and 110 m depth from 25 CTD (conductivity, temperature, depth) casts in and around the Nazaré Canyon (Figure 3.1, Appendix D). Physical oceanographic, biological and chemical data (i.e. temperature, salinity, turbidity, fluorometry and nutrients) and water column samples were collected using a combined Neil Brown MKIIIC CTD profiler equipped with an Aquatracka nephelometer, a Seapoint fluorometer and a rosette sampler (12 Niskin bottles of 8 litres). 192 suspended matter samples were collected from surface, intermediate and bottom nepheloid layers in order to define the particulate matter concentration (PMC) and to calibrate the nephelometer response (turbidity). The PMC (g/m3) was compared to a laboratory calibration of the instrument with a standard formazine solution (FTU). The turbidity calibration for March 2010, was FTU = 0.112*PMC with r = 0.88.

3.3.2. Meteorological and hydrological data

Hydrographic conditions during the cruise as determined from CTD profiles are represented as contour plots using inverse distance to power gridding in Surfer Version 8 software. A WSW-ENE oriented transect covering the entire length of the upper-middle Nazaré Canyon axis (23 CTD casts) was built to represent density, temperature, salinity and turbidity conditions during the sampling period (casts indicated in Figure 3.1; CTD profiles in Figures 3.2a-d). For a more detailed description of the data referring to wind, sea wave, and river discharge and sky conditions, the reader is referred to Guerreiro et al. (2013).

3.3.3. Satellite data

Monthly averaged surface water chlorophyll a (Chl-a) concentration between 2006 and 2011 was assessed from satellite data as a framework for interpreting spatial and temporal distribution of phytoplankton in the Nazaré Canyon. Chl-a data acquired by the Moderate- resolution imaging spectroradiometer (MODIS) on NASAs Aqua satellite and processed by The Ocean Biology Processing Group (OBPG) were downloaded from the Ocean Color Website (http://oceancolor.gsfc.nasa.gov/). After quality checking and masking, valid data were interpolated from a grid of regular latitude-longitude intervals. For each image, with nominal resolution of 1 km, data corresponding to three defined transects (one transect along the canyon, two other crossing it) were extracted and averaged per month.

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Figure 3.1– Geographical location of the study area and investigated CTD casts. Number labelled stations indicate locations where samples for coccolithophore analysis were collected.

Influence of the Nazaré Canyon

3.3.4. Laboratory and microscope analysis

3.3.4.1. Coccolithophores

For the study of coccolithophores, seawater samples of around 2 l were filtered over cellulose acetate filters (47 mm diameter and 0.45 μm pore size) using a low pressure vacuum system. The filters were then rinsed with tap water to remove salt and oven-dried at 40 ºC for 24 hours. A randomly chosen section (approx. 30–45º) of each filter was cut and permanently mounted on a glass slide. Coccospheres (cells) were identified and counted under polarized light microscope (PLM) (Olympus BX-40) at 1250× magnification. The scanned area per filter varied between 0.1 and 3.5 mm2, depending on the general cell density. The number of cells per liter of seawater was estimated from the number of counted coccospheres multiplied with the ratio of filled filter area to observed area and divided by the volume of filtered water (Cros, 2001). For the study of the living assemblages (cells) only the water column between 5 and 110 m water depth was considered. To refine the taxonomic differentiation of Alisphaera spp., Algirosphaera robusta, Gephyrocapsa spp., Ophiaster spp., Syracolithus dalmaticus and Syracosphaera spp., 13 samples were investigated using Scanning Electron Microscope (SEM Hitachi S-3500N, at 5 kV). Samples were selected for containing relatively higher cell densities and species diversity. A randomly chosen section of the selected filters was fixed with colloidal Ag on a SEM stub and sputtered with an Au-Pd coating of maximum 20 nm thick; then, a minimum number of 100 vision fields (VF) were observed and counted using magnifications between 1000× (observation area of each VF: 126.52 × 94.84 μm) and 2000× (observation area of each VF: 63.26 × 47.42 µm). Identification of coccolithophore species followed Jordan et al. (2004) and Young et al. (2003), whilst the new website on nannoplankton taxonomy http://nannotax.org (Young et al., 2011) and specific literature on light microscopy (Frada et al. 2009), Mediterranean coccolithophores (Cros and Fortuño 2002) and Syracosphaera genus (Kleijne and Cros, 2009) provided useful additional guidance for classification.

3.3.4.2. Phytoplankton pigments (Chl-a) and nutrients

Chl-a concentrations were used as an indicator for phytoplankton biomass. Water samples of 2 l were filtered over Whatman GF/F filters (0.7 μm pore size, 25 mm diameter), and the filters were immediately deep-frozen and stored at −80 °C. Phytoplankton pigments were extracted with 2-3 ml of 95 % cold-buffered methanol (2 % ammonium acetate) and analysed with high-performance liquid chromatography (HPLC). Chromatographic separation was carried out following Zapata et al. (2000). Chl-a concentrations obtained from 25 HPLC samples were then used to calibrate fluorometry measurements obtained from CTD casts (r2 =0.7, with p <0.01). Nutrient concentrations (nitrate, nitrite, ammonium, phosphate and silicate) were determined using a Skalar SANplus Segmented Flow AutoAnalyzer specially developed for the

93 Chapter 3

analysis of saline waters. N–NOx and N–NO2 were determined according to Strickland and

Parsons (1972), with N–NO3 being estimated by the difference between the previous two; N–

NH4 and Si–SiO2 were determined according to Koroleff (1976); P–PO4 was determined according to Murphy and Riley (1962). All methods were adapted to the methodology of segmented flow analysis and uncertainties were determined following Mendes et al. (2011).

3.3.5. Statistical analysis

A statistical multivariate analysis (r-mode Factor Analysis by Statistica 10) was performed upon the data matrix with coccolithophore cell densities, nutrient concentrations

(NOx, PO4, SiO2), biomass (fluorometry calibrated with Chl-a concentrations measured by HPLC) and physical parameters (temperature, salinity, turbidity) as columns (variables). Results from the original data matrices were optimized through Varimax Raw rotation.

3.4. Results

3.4.1. Environmental conditions during the cruise

The plankton cruise took place under transient environmental conditions in late winter 2010, as discussed in detail in Guerreiro et al. (2013) (Chapter 2). Sampling was performed at the end of an unusually cold winter in Europe (2009–2010) under an exceptionally negative phase of the North Atlantic Oscillation (NAO) (Cattiaux et al., 2010; Troupin and Machin, 2012). Whilst a northerly wind regime began to settle around the start of the cruise, the winter mixed layer was still occupying most of the water column over the shelf and upper slope (uppermost ~150–200 m water depth), as normally the case during winter off Portugal (Oliveira et al., 2004). However, intense river runoff that occurred prior to and continued during the cruise had produced a well-established colder and less saline surface layer extending from near the coast to more than 50 km offshore, overlying the warmer and saltier winter mixed layer waters (Figures 3.2a,b,c). The lowest TS values within this buoyant plume fed by runoff water were measured at the surface, approximately between 16 and 30 km off the coast (stations 79 and 122, respectively). The warmer and saltier winter mixed layer associated with the flow of the IPC along the Portuguese margin was noticeable below the surface buoyant plume in the entire investigated region, generally below 15-20 m water depth, appearing continuous in north-south direction close to the shelf-break, at the upper-middle Nazaré Canyon transition. Further offshore it was mostly noticed along the southern flank of the middle canyon but weakening northwards where significant mixing apparently occurred with colder water masses from north. The TS contrast between the superficial BP and the winter mixed layer below was particularly pronounced in the upper Nazaré Canyon where the core of the IPC penetrated up-canyon to less than 10 km off the coast. TS profiles along the canyon axis show evidence of strong vertical oscillation around

94

Figure 3.2 – Density (a), salinity (b), temperature (c) and turbidity (d) sections obtained from CTD casts along a WSW-ENE transect representing the hydrological conditions during the cruise along the upper-middle Nazaré Canyon axis. Labels refer to stations where plankton samples were collected for coccolithophore studies.

Chapter 3

Belatina Valley (station 120) possibly driven by internal tides in this part of the canyon (Quaresma et al., 2007) (Figures 3.2a,b,c). Turbidity was generally low, with relatively higher FTU values noticed in the surficial water layer, as well as at the bottom layer of the upper canyon (i.e. in the canyon head and close to the intersection with Vitória tributary). Highest turbidity values recorded around 200–300 m water depth appear to reflect bottom sediment resuspension caused by the canyon’s internal tide (Figure 3.2d). Highest nutrient concentrations were recorded in the relatively cool and low-saline surface water of the BP, decreasing to lower concentrations in the winter mixed layer water underneath. The vertical decreasing trend was particularly noticeable in the case of SiO2 (Figure

3.3). NOx/PO4 ratio was generally close to the 16:1 Redfield Ratio typical for marine waters

(Redfield et al., 1963). A slight deviation toward lower NOx concentrations relative to PO4 in most samples suggests that NOx was the major limiting nutrient for phytoplankton growth at that time. Phytoplankton biomass inferred from Chl-a concentrations (max. <0.7 µg/l) was generally low during the cruise, with the highest values reached at the uppermost part of the water column (above 50 m depth) (Figure 3.4). Highest Chl-a and nutrient concentrations (NOx and SiO2) and the lowest salinities were measured at the surface (5 m) near Belatina Valley (stations 118 and 120) and north of the upper canyon (stations 112 and 111).

Figure 3.3 - Relationship between nutrient concentration and salinity during the cruise. Water depths were not differentiated in this analysis (i.e. nutrient data between 5 – 110 m water depths were plotted all together).

96 Influence of the Nazaré Canyon

Figure 3.4 – Vertical distribution of phytoplankton biomass (Chl-a), salinity and nutrients along the uppermost 110 m water depth, during the cruise. Grey squares refer to biomass and black squares represent salinity and nutrient concentrations.

3.4.2. Coccolithophores

4.4.2.1. Species diversity, cell density and distribution

A total of 35 distinct taxa of coccolithophores (coccospheres) were recognized. 19 species and 4 genera were identified using polarizing light microscopy (PLM) whereas additional Scanning Electron Microscope (SEM) analysis revealed an additional 16 species belonging to the genera Syracosphaera, Ophiaster, Alisphaera and Acanthoica, and one holococcolithophore, Syracolithus dalmaticus (see Table 3.1). The list of observed species is presented in Appendix A. Coccolithophore cells occurred within the BP and the upper layers of the winter mixed layer as indicated in Figure 3.5. Total cell densities ranged between 4.0×103 and 6.0×105 cells/l (Table 3.1). The highest cell densities along a transect covering the upper-middle Nazaré Canyon axis were noticed close to Belatina Valley, associated to minimum TS values within the BP (stations 118 and 120) (Figure 3.6). High cell densities were also noticed closer to the coast, at the canyon’s head (station 87), less than 2 km off the coast, and above the southern canyon rim (station 89) (Figure 3.7a). Further offshore toward the open ocean (station 132) lower cell densities were observed, distributed more homogeneously over the water column (Figure 3.7b- c). Of the 35 identified taxa, only ten reached significant cell densities of more than 2000 coccospheres per litre: Emiliania huxleyi, Syracosphaera spp., Gephyrocapsa ericsonii, G. oceanica, G. muellerae, Coronosphaera mediterranea, Ophiaster spp., Helicosphaera carteri, Syracolithus dalmaticus and Algirosphaera robusta. E. huxleyi was the dominant species during the cruise, particularly at the surface close to the shelf-coastal region (Figure 3.8, Table 3.1). Below the surface and further offshore, other species gained in relative importance within the total assemblage, generally displaying a broader vertical distribution (Figure 3.9; Guerreiro al., 2013) (Chapter 2). G. ericsonii, A. robusta, Acanthoica spp., Syracosphaera pulchra, S.

97 Chapter 3

Figure 3.5 - Coccolithophore cell densities (cells/l) observed during the cruise plotted over a TS diagram. Solid lines refer to CTD profiles from selected stations to illustrate the surface mixed layer and the ENACWst as defined by Fiúza (1984) and Fiúza et al. (1998): stations 87, 118 and 132 located at 225 m, 854 m and 3478 m water depths, respectively.

dalmaticus, Coccolithus pelagicus, Michaelsarsia elegans and, to a lesser extent G. oceanica, displayed a downward decreasing trend in cell density, similar to that of E. huxleyi. Other groups of species such as Syracosphaera spp, Ophiaster spp. and Gephyrocapsa muellerae revealed a more uniform vertical distribution. The remaining taxa did not reveal a specific vertical distribution pattern (Figure 3.8). A coast to open ocean ecological and hydrological dichotomy is well illustrated in Figure 3.9: E. huxleyi dominated at the surface in coastal waters (stations 87 and 120, Figures 3.9c,b), whereas Syracosphaera spp. and Ophiaster spp. were dominant further offshore in more open- ocean conditions, and showing a broader vertical distribution (station 132, Figure 3.9a). Closer to Belatina Valley, the three taxa co-existed, with E. huxleyi largely dominating at the surface, and the latter taxa relatively increasing in the subsurface water mass (Figure 3.9b). G. muellerae, G. oceanica and S. dalmaticus were also more abundant near the coast, whereas G. ericsonii and C. mediterranea revealed a broader lateral distribution.

98 Influence of the Nazaré Canyon

Table 3.1 – Maximum cell densities (cells/l) of the coccolithophore species observed under PLM during the sampling period. The respective water depth, sampling station and location are indicated (BNL = bottom nepheloid layer ≤ 110 m water depth). Minimum and maximum values of total cell densities, temperature, salinity, turbidity, fluorometry, Chl-a measured by HPLC, phytoplankton biomass and nutrients (NOx, PO4 and SiO2,) are indicated below. NC = Nazaré Canyon.

Taxa Cells/l Level Station Location mean max.

Acanthoica spp. 166 1134 5 85 NC head Algirosphaera robusta 294 2049 5 101 South of upper NC Alisphaera spp. 56 1152 50 87 NC head Calcidiscus leptoporus 38 1814 BNL 96 NC head northern rim Coccolithus pelagicus 42 726 5 132 Middle NC Coronosphaera mediterranea 782 4536 BNL 94 North of upper NC Discosphaera tubifera 6 605 50 87 NC head Emiliania huxleyi 9950 39827 5 118 Belatina valley Gephyrocapsa ericsonii 3932 10916 5 118 Belatina valley Gephyrocapsa muellerae 1581 9466 50 98 NC head Gephyrocapsa oceanica 584 3893 15 111 North of upper NC Helicosphaera carteri 135 5184 BNL 93 NC head northern rim Michaelsarsia elegans 9 382 5 85 NC head Ophiaster spp. 1468 5544 25 132 Middle NC Palusphaera vandelii - 393 25 98 NC head Rhabdosphaera clavigera 6 298 5 111 North of upper NC Scyphosphaera apsteinii 12 889 BNL 111 North of upper NC Syracolithus dalmaticus 110 3209 25 115 Vitória tributary Syracosphaera spp. 2477 8951 5 132 Middle NC Syracosphaera pulchra 17 789 5 110 North of upper NC Umbellosphaera cf. irregularis 5 246 50 122 Upper NC axis Umbilicosphaera hulburtiana 19 1779 25 120 Belatina valley Umbilicosphaera sibogae 49 1120 50 132 Middle NC min. max. Total cells/l 3629 59888 Fluorometry (µm/l) 0.11 1.02 Chl-a (µm/l) 0.06 0.69 Biomass (µm/l) 0.15 0.63 NOx (µmol/l) 2.3 9.7

PO4 (µmol/l) 0.12 0.88

SiO2(µmol/l) 1.7 10.7 Temperature (ºC) 13.9 15.04 Salinity 34.05 36.2 Turbidity (FTU) 0.02 0.19

99 Chapter 3

Figure 3.6 - Coccolithophore total densities (cells/l) and isopycnals (kg/m3) recorded in the uppermost 110 m water depth along a WSW – ENE oriented transect covering the upper-middle Nazaré Canyon axis. Black arrows indicate the highest cell densities at the surface: stations 120 and 118 close to Belatina Valley, and station 87, at the canyon head.

4.2.2. Multivariate analysis

Results from factor analysis revealed four distinct factor assemblages explaining 46 % of the total variance in the data (Table 3.2, Figure 3.10). Factor 1 (F1) explains 22 % of total variability, with NOx, SiO2, Acan and Eh recording the highest (positive) factor loadings, in opposition to S, T (and Syraco and Ophi) (negative loadings). Factor 2 (F2) explains 10 % of total variance, being represented by Ge, Biom and Cm (and Eh) (positive loadings). Factor 3

(F3) explains 8 % of total variability and is represented by Dtub, Alisph (and PO4) (negative loadings). Factor 4 (F4) explains 7 % of total variability and it is represented by Go (and Turb) (positive loadings) in opposition to Meleg (negative loadings).

Samples influenced by factor assemblage NOx, SiO2, Acanthoica spp. and E. huxleyi (F1 positive scores) were better represented at the surface, particularly close to Belatina Valley (stations 118 and 120) but also around the uppermost reaches of the Nazaré Canyon (stations 112, 111, 102) and the canyon head (stations 85, 87) (Figure 3.10a). Below the surface this assemblage was practically inexistent or weakly represented. Samples influenced by salinity, temperature, Syracosphaera spp. and Ophiaster spp. (F1 negative scores) were preferentially represented further offshore and showed a relatively broader lateral distribution, and at Belatina Valley region below the surface (Figure 3.10a). Samples influenced by G. ericsonii, phytoplankton biomass (Chl-a), C. mediterranea (and to a lesser extent, E. huxleyi) (F2 positive scores) revealed a rather broad lateral

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Figure 3.7 – Coccolithophore total densities (cells/l) and isopycnals (kg/m3) recorded along four transects cutting across the Nazaré Canyon upper reaches, approximately SSW – NNE oriented: T1 (a) is located at the canyon head and T4 (b) represents the more distal section.

Figure 3.8 - Vertical distribution of the most common coccolithophore taxa along the uppermost 110 m water depth.

Figure - 3.8 (cont.)

Figure 9 – CTD/turbidity and fluorometry casts and coccolithophore assemblages living in the uppermost 100 m of three selected stations monitored during the cruise: (a) station 132 located at the middle Nazaré Canyon (3478 m), (b) station 118 located near Belatina Valley (854 m), and (c) station 87 located at the Nazaré Canyon head (224 m). Fluorometry was calibrated with in situ Chl-a measurements.

Chapter 3 distribution, preferentially at the uppermost 25 m in the Nazaré Canyon head and at Belatina Valley, whereas further offshore a broader vertical distribution is noticed (Figure 3.10b).

Samples influenced by Discosphaera tubifera, Alisphaera spp. and PO4 (F3 negative scores) recorded their strongest signal at 50 m water depth, at the Nazaré Canyon head (station 87) (Figure 3.10c). Samples influenced by G. oceanica and turbidity (F4 positive scores) were consistently distributed in more neritic-coastal regions, particularly at the canyon head and surroundings (stations 87, 93), at all water depths. In the intersection between the canyon axis and Vitória tributary (station 80) and at Belatina Valley, this assemblage was well represented at the uppermost 25 m (Figure 3.10d). The relatively low percentage of variance explained by F1-F4 (< 50%) reflects the highly transient meteorological and hydrological conditions during the cruise, where water masses (both oceanic and continental) were still adjusting to the circulation imposed by the shifting wind regime (see Guerreiro et al., 2013). Nevertheless, factor analysis helped to reveal and understand the most important ecological signals during the cruise: (a) coccolithophore cell density and diversity “hotspot” at the Nazaré Canyon head, despite of abundant detritic material (i.e. terrigenous particles, reworked coccoliths). Significant amounts of perfectly preserved cells, particularly of E. huxleyi, together with several other species, testify of the high diversity found in this part of the canyon (see Appendix B). Gephyrocapsa muellerae, Syracolithus dalmaticus, Acanthoica spp. and Michaelsarsia elegans had their maxima in this area (Table 3.1). Additional SEM observations confirmed the relative increase of Calcidiscus leptoporus, Coccolithus pelagicus and Helicosphaera carteri in the canyon head, together with the single occurrence of Syracosphaera amoena (formerly S. bannockii, see Dimiza et al 2008), Syracosphaera molischii, Palusphaera vandelii and Syracosphaera anthos. G. oceanica was also systematically better represented in the canyon head at all water depths, associated to turbidity; (b) Stations close to Belatina Valley seemed to represent a nutrient, Chl-a and coccolithophore “hotspot”, with E. huxleyi, G. ericsonii, C. mediterranea (and G. oceanica) dominating the assemblages at the uppermost 25 m water depth, and Syracosphaera spp. and Ophiaster spp. dominating underneath; (c) E. huxleyi was clearly displaced towards the neritic/coastal zone, and G. ericsonii and C. mediterranea more towards the neritic-oceanic zone. Syracosphaera spp. and Ophiaster spp. were consistently better represented below the surface and further offshore.

104 Influence of the Nazaré Canyon

Table 3.2 - Results from factor analysis: eigenvalues and explained variance obtained for the samples collected during the sampling period. The more significant variables were: temperature (T), salinity (S), turbidity (Turb), Chl-a, nutrients (NOx, PO4 and SiO2), Acanthoica spp. (Acan), Alisphaera spp. (Alisph), C. mediterranea (Cm), D. tubifera (Dtub), E. huxleyi (Eh), G. ericsonii (Ge), G. oceanica (Go), M. elegans (Meleg), Ophiaster spp. (Ophi), and Syracosphaera spp. (Syraco).

Factor 1 Factor 2 Factor 3 Factor 4 Acan 0.7 0.1 0.0 -0.4 Arob -0.1 0.2 0.1 0.2 Alisph -0.2 0.1 -0.9 0.0 Cl -0.3 0.2 0.1 -0.2 Cm 0.3 0.6 0.0 0.2

Cp 0.0 0.3 0.0 -0.3

Dtub 0.0 -0.1 -0.9 0.1 Eh 0.6 0.5 0.0 0.3 Ge 0.1 0.8 0.1 0.0 Gm 0.1 -0.2 0.3 0.1 Go 0.0 0.0 0.0 0.7 Hc -0.1 -0.1 0.1 0.3 Meleg 0.4 -0.1 0.1 -0.5

Ophi -0.5 0.4 -0.1 -0.4

Rhab 0.4 0.4 0.0 0.0 Spul 0.0 -0.2 0.0 -0.1 Sypho -0.1 0.0 0.0 0.0 Usib 0.0 -0.1 0.0 0.1 Syraco -0.5 0.4 0.0 -0.2 Sdalm 0.4 -0.2 0.1 0.0 T -0.9 0.1 0.0 -0.1 S -0.9 -0.2 0.0 0.0

Turb 0.5 0.0 0.0 0.5 Chl-a 0.3 0.7 0.0 -0.3

NOX 0.9 0.1 0.0 0.0 PO4 0.5 -0.1 -0.7 -0.1 SiO2 0.7 0.1 0.0 -0.1 Eigenvalues 5.9 2.7 2.2 1.7 Total variance (%) 21.8 10.0 8.0 6.5

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Figure 3.10 - Water column density section (kg/m3) for a transect along the upper-middle Nazaré Canyon, with spatial distribution of scores from Factor 1 (a), Factor 2 (b), Factor 3 (c) and Factor 4 (d) obtained from the coccolithophore data. In each association species/variables are aligned according to their factor loadings (in brackets those with less importance) and coded as an equation: numerator = positive loadings; denominator = negative loadings. For taxonomic complete references see Table 3.2.

Influence of the Nazaré Canyon

3.4.3. Monthly averaged Chl-a from satellite imagery

Time-series of monthly averaged Chl-a between 2006 and 2011 calculated from satellite data are shown for three transects: transect A, WSW–ENE oriented, covering the whole upper- middle canyon axis (Figure 3.11a); transect B, N–S oriented, cutting across the canyon axis at Belatina Valley (station 120) (Figure 3.11b); and transect C oriented at a low angle to the coastline and cutting across the canyon head (station 87). The along-canyon time series (Figure 3.11a) illustrates the recurrent maximum of Chl-a in offshore waters occurring around March and April of all years, and a more persistent presence of high Chl-a concentrations in the coastal zone during spring and summer months. There is no evidence of persistent or particularly high Chl-a at Belatina Valley, although the transition zone between Chl-a enriched waters extending from the coast and Chl-a poorer offshore waters is often located approximately in this region. A map of average Chl-a concentration for March 2010 (see Figure B in Auxiliary Material, Chapter 2) illustrates the broad spatial spread of this Chl-a enrichment, occupying a significant portion of the continental shelf and extending approximately up to the middle shelf region, apparently coming from north. Slightly higher Chl-a concentrations are noticed along the canyon axis in comparison to the shelf immediately north of it, particularly at Belatina Valley, where the highest coccolithophore cell densities and Chl-a were recorded in situ during the cruise. Similar offshore outbreaks of Chl-a enrichment were also observed in March 2006 and 2009, extending almost to the shelf- break in 2006, and even beyond in 2009 (data not shown).

Figure 3.11 – Monthly averaged Chl-a production in the Nazaré Canyon region during 2006-2011, obtained from satellite data: (a) along-canyon oriented Transect A, between 39.59N, -9.1W and 39.51N, -9.9W; (b) north-south oriented Transect B crossing the canyon at station 120, between 39.85N, -9.41W and 39.2N, -9.41W; and (c) NNE-SSW oriented Transect C crossing the canyon at station 87, between 39.85N, -9.1W and 39.4N, -9.41W. Dashed black lines indicate the location of stations 87, 118 and 120.

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Figure 3.11a – Monthly averaged Chl-a production in the Nazaré Canyon during 2006-2011, obtained from satellite data along-canyon oriented (Transect A). Dashed black lines indicate the location of stations 87, 118 and 120.

Figure 3.11b – Monthly averaged Chl-a production in the Nazaré Canyon during 2006-2011, obtained from satellite data: N-S oriented Transect B crossing the canyon at station 120. Dashed black lines indicate the location of station 120.

Figure 3.11c – Monthly averaged Chl-a production in the Nazaré Canyon during 2006-2011, obtained from satellite data, NNE-SSW oriented Transect C crossing the canyon at station 87. Dashed black lines indicate the location of station 87.

Influence of the Nazaré Canyon

The Chl-a time series for the transect across the canyon at Belatina Valley (Figure 3.11b) shows higher concentrations in the canyon meander and adjacent northern and southern shelf in March of 2006, 2009 and 2010, reflecting the seasonal offshore spread of Chl-a enrichment. Chl-a concentrations are consistently higher south of 39.4 N where the transect is located in the more productive near shore area, whereas concentration is much lower along the northern part of the transect located in the less productive offshore area. Persistently high Chl-a concentration is observed close to the coast, particularly in spring and summer months (between March and October), reaching the highest concentrations in August-October 2007, and June-September 2010. The time series for the NNE-SSW near-shore transect cutting across the canyon head (Figure 3.11c) shows maximum Chl-a concentrations in the canyon head and immediate vicinity in these time-intervals, exceeding concentrations on the surrounding shelf. The timing of Chl-a peaks in the canyon head, between mid-August and mid- September 2007; between mid-May and mid-June 2009; in March and between mid-June and mid-August 2010, is conspicuously different from that of the widespread Chl-a enrichment in early spring extending across the shelf.

3.5. Discussion

3.5.1. Late winter coccolithophore assemblages off Portugal

Moderately low coccolithophore cell densities (between 3.6×103 and 6×105 cells/l) and low phytoplankton biomass (Chl-a) (max. <0.7 µg/l) were observed during the sampling period, which is in good agreement with observations by Moita (2001) and Silva et al. (2009) regarding wintertime phytoplankton production off Portugal. The lack of a clear correlation between Chl-a and nutrients (Figure 3.4) suggests that phytoplankton production was generally low and not limited by nutrient availability within the BP. In comparison, previous studies reporting a much stronger relationship with nutrient concentration attributed a decisive role to haline-stratification in promoting phytoplankton blooms during late winter upwelling events off Portugal (Peliz and Fiúza, 1999; Ribeiro et al., 2005; Santos et al., 2004). The subdued phytoplankton growth here observed is interpreted as resulting from important advective mixing promoted by the BP during this period of intense runoff, sub-optimal light conditions due to cloud cover and initial relatively high turbidity within the superficial BP (discussed in Guerreiro et al., 2013) (Chapter 2). Four distinct ecological signatures (factors) were extracted from multivariate statistical analysis applied to the present dataset, explaining 46 % of the variability within the data and revealing the most important environmental and ecological signals during the cruise (Figure 3.10, Table 3.2). Factor 1 (positive loadings) is interpreted as representing the gradient between the runoff- influenced coastal-neritic zone, where relatively high nutrient concentrations were retained in the superficial BP, and the oceanic mixed water that characterizes the Portuguese margin during

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Chapter 3 winter, present below the BP closer to the coast and surfacing further offshore. Acanthoica spp. and Emiliania huxleyi appear positively correlated with nutrients at the surface within more coastal-neritic conditions. F1 was strongly expressed close to Belatina Valley and around the Nazaré Canyon head and surroundings, but nearly absent below the surface, highlighting the strong vertical density gradient of the BP and the clear preference of these taxa to develop at the sunlit nutrient-rich surface water layer (Figure 3.9b,c and 3.10a). The large dominance of E. huxleyi at the less saline sunlit surface layer and its preference for more coastal/neritic conditions is in good agreement with several authors describing this species as having a highly cosmopolitan distribution independent of sea surface temperature, and attaining high cell densities in both oligotrophic and eutrophic environments (Andruleit, 2007; Baumann et al., 2000; Winter et al., 1994). This species was considered to be a possible indicator for more stable regions regarding with nutrient availability (Andruleit and Rogalla, 2002), and is often found associated with nutrient-rich and productive coastal regions (e.g. Andruleit, 2007; Giraudeau and Bailey, 1995; Sprengel et al., 2002; Silva et al., 2008). From various locations it has been reported as responsible for major blooms (e.g. Garcia et al., 2011; Knappertsbush and Brummer, 1995). E. huxleyi was also weakly positively correlated to Gephyrocapsa ericsonii, Coronosphaera mediterranea and Chl-a in Factor 2 (positive loadings), particularly in what revealed to be the most productive station monitored during the cruise, located around Belatina Valley (Figure 3.10b). Further offshore where E. huxleyi was not dominating the coccolithophore community, the two taxa were also important. G. ericsonii was the second most abundant species during the cruise, next to E. huxleyi, which is in good agreement with several studies indicating its preference for nutrient-enriched coastal-neritic regions (Giraudeau and Bailey, 1995; Silva et al., 2009; Winter et al., 1979). C. mediterranea was also significantly present during the cruise, supporting previous observations reporting high cell densities of this species off the Nazaré region (Moita et al., 2010; Silva et al., 2008), and fast response to nutrient availability in this area during winter (Guerreiro et al., 2013) (Chapter 2). On the contrary, Syracosphaera spp. and Ophiaster spp. (negative loadings of Factor 1) showed a higher affinity for warmer and saltier open ocean waters, and these species appeared more broadly distributed along the water column (Figures 3.9a and 3.10a). Closer to the coast, these species were generally less frequent, although higher cell densities were observed below the surface, where they were apparently able to compete with E. huxleyi. This suggests that the lower light and nutrient level within neritic subsurface waters were less limiting for these taxa than for E. huxleyi. Results are consistent with Andruleit (2007) in terms of the broad depth range of Syracosphaera spp. but not concerning the affinity of this group for nutrient availability in coastal regions as reported in earlier studies (e.g. Andruleit, 2007; Andruleit and Rogalla, 2002; Giraudeau and Bailey, 1995). Whereas SEM observations indicated that Syracosphaera marginoporata was the dominant species within the group (max.1.4×105 cells/l), the low level of taxonomical differentiation of Syracosphaera spp. from the above mentioned studies may explain the discrepancy between its reportedly association with relatively eutrophic conditions and its preferential distribution in the relatively oligotrophic oceanic waters of the

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Nazaré Canyon region. The same applies to Ophiaster spp. of which little is known yet in terms of both ecological preferences and biogeographic distribution. Whereas our late winter observations seem to indicate an association of this genus with oceanic-oligotrophic conditions, other studies describe it as associated to nutrient-rich environments such as subtropical frontal zones and upwelling areas (e.g. Boeckel and Baumann, 2008; Kleijne, 1993). Discosphaera tubifera and Alisphaera spp. were not abundant during the cruise (<2000 cells/l), and found weakly correlated to PO4 (negative loadings of Factor 3), very close to the coast at the Nazaré Canyon head (station 87, 50 m water depth) (Figure 3.10c). In the recent literature, D. tubifera is typically associated with subtropical gyres (Boeckel and Baumann, 2008) and oligotrophic waters, always outside the upwelling area (e.g. Andruleit et al., 2003; Kleijne, 1992). Ecological preferences of Alisphaera spp. are still poorly known, whereas Kleijne (1993) found it associated with G. oceanica in the warm waters of the Indian Ocean and Sourthern Red Sea, both increasing towards the central upwelling zone. In addition to these taxa, the sporadic occurrence of other species of subtropical affinity in the upper Nazaré Canyon, i.e. Rhabdosphaera clavigera, Palusphaera vandelii, Umbellosphaera irregularis, Scyphosphaera apsteinii and Umbilicosphaera hulburtiana, and the local relative increase of species that exhibited an oceanic affinity during the cruise, i.e. Calcidiscus leptoporus, Coccolithus pelagicus, Syracosphaera amoena, and Syracosphaera molischii were also noticed. The relatively oligotrophic signature of coccolithophore assemblages observed in subsurface waters along the Nazaré Canyon axis seems in favour of the hypothesis that the canyon acts as a preferential pathway for advection of oceanic waters derived from ENACWst from offshore onto more nearshore areas during winter (see section 3.5.2). Gephyrocapsa oceanica appears to be related to turbidity, although the correlation is somewhat weak (positive loadings of Factor 4). This species was consistently distributed closer to the coast (< 10 km) at all water depths, particularly at the canyon head and adjacent shelf (Figure 3.10d). The broad depth range of G. oceanica was also recognized by Andruleit (2007) and Houghton and Guptha (1991), as well as its tolerance for lithogenic particles, which would be in accordance with the occurrence of G. oceanica in the dynamic canyon head area; water samples collected from this area displayed a highly content in terrigenous particles and reworked coccoliths; see Appendix B, Figures 45 and 46). The coastal preference of G. oceanica is also in good agreement with Silva et al. (2008) and Guerreiro et al. (2013; submitted-b) (Chapters 2 and 4), who described this species as a typical coastal coccolithophore, well adapted to the nutrient-rich and productive environment off Portugal. The species seems able to quickly respond to nutrient input (Andruleit and Rogalla, 2002; Andruleit et al., 2003; Broerse et al., 2000; Giraudeau and Bailey, 1995; Sprengel et al., 2002; Winter et al., 1994). The relatively low cell densities of this species confirm the generally low-productive conditions during the cruise.

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3.5.2. Influence of the submarine canyon and hydrological conditions

Although phytoplankton production apparently had not yet responded to higher nutrient availability provided by runoff, as revealed by generally low coccolithophore cell and Chl-a concentrations (see section 2.5.1 in Chapter 2, Guerreiro et al., 2013), local abundance and diversity “hotspots” were noticed in the upper Nazaré Canyon axis close to Belatina Valley (stations 120 and 118) and in the canyon head (station 87). Of particular interest for the canyon head dynamics are the sporadic occurrences of typical subtropical-oligotrophic species, such as Discosphaera tubifera and Palusphaera vandelii. These species were only observed in this proximal part of the canyon and may be interpreted as tracers for the preferential onflow of ENACWst through the upper canyon during winter, as revealed by TS profiles along the Nazaré Canyon axis (Figures 3.2a,b). Shoreward deflection of circulation in the upper water column is expected to be stronger when the water column above the shelf and upper slope is relatively unstratified (see Allen, 1996; She and Klinck, 2000), as typically the case off Portugal during this time of the year (Oliveira et al., 2004). Along with these subtropical species, a diverse assemblage dominated by the productive Emiliania huxleyi, Gephyrocapsa ericsonii and Coronosphaera mediterranea was observed in the canyon head. Maxima of other species, both neritic-coastal (i.e. Gephyrocapsa oceanica, Acanthoica spp.) and neritic-oceanic (i.e. Gephyrocapsa muellerae, Syracolithus dalmaticus and Alisphaera spp.) were also observed in this area. Whereas during the low productive winter season the shoreward advection of oceanic waters through the canyon can be traced by relatively diverse coccolithophore assemblages with oligotrophic subtropical affinity, satellite data clearly show a maximum in Chl-a concentration at the canyon head between March and October suggesting that upwelling of oceanic waters in the canyon head enhances phytoplankton productivity making the canyon head the most persistently productive part of the inner shelf zone (Figures 3.11a,c). Also during the years of lower productivity a relative increase of Chl-a is noticed at the canyon head. Previous observations from Mendes et al. (2011) had already indicated that the highest Chl-a concentrations during an upwelling event occurred at the canyon head (> 4 μg/l). Enhanced Chl-a concentrations observed in satellite imagery south of the Nazaré Canyon and close to Cape Carvoeiro supports previous observations of Mendes et al. (2011) of persistently high concentrations of diatoms in this area, interpreted as reflecting the occurrence of intensified upwelling along the southern canyon rim extending its influence over the southern shelf, and persisting even during relaxation of upwelling-favourable winds. Enhancement of upwelling in the canyon head and nearby shelf is in accordance with studies of Bosley et al. (2004), Hickey (1995) and Skliris and Djenidi (2006). However, the recurrent generation of upwelling filaments off Cape Carvoeiro during spring-summer should also be considered when explaining high production of phytoplankton in this area (e.g. Fiúza, 1983; Haynes et al., 1993; Peliz et al., 2002). The region close to Belatina Valley, where the upper canyon axis makes a tight turn

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(stations 120 and 118), also stood out for particular hydrological and ecological characteristics. The highest phytoplankton biomass and coccolithophore cell densities during the cruise were observed in this area, with E. huxleyi, G. ericsonii and C. mediterranea dominating the assemblage in the uppermost 25 m of the water column. The lowest TS values and the highest nutrient concentrations within the superficial BP were also measured here, whereas indications of enhanced vertical baroclinic oscillation were noticed underneath the BP (Figures 3.2a,b), interpreted as resulting from the interaction of internal waves with the canyon topography. The conversion of barotropic to baroclinic tidal motion occurs in the presence of water stratification and leads to the generation of internal (baroclinic) tides (i.e. internal waves of tidal period), which radiate from the generation point and propagate the tidal energy vertically (Quaresma et al., 2007; Tyler et al., 2009). The vertical density gradient existing between the BP (above) and the ENACWst (below) within the confined topography of the upper canyon will likely promote the baroclinic oscillation of the water masses involved. In addition, the presence of a meander in this part of the canyon axis appears to block the flow of the internal wave, leading to local amplification of the vertical oscillation. One could speculate that this represents a typical hydrological feature of the canyon during wintertime, given that it is during this time of the year that the IPC usually surfaces and reaches particularly nearshore areas within the canyon. During summer, when the IPC retreats down to slope water depths, baroclinic activity near the surface is mainly associated to water column thermo-haline stratification typical of this season (e.g. Quaresma et al., 2007). The highest cell and Chl-a concentrations measured in situ close to Belatina Valley may be interpreted to merely represent a local expression of shelf-wide high phytoplankton production recurrently occurring during the month of March (Figures 3.11a and Figure B in Auxiliary Material, Chapter 2). Although slightly higher monthly Chl-a concentrations appear to be roughly aligned with the canyon axis in comparison to the northern shelf, in particular close to the meander (Figure B-b in Auxiliary Material, Chapter 2), it is very hard to decipher whether this reflects a recurrent physical phenomenon related to the canyon or merely an artefact produced by the satellite acquisition. Given that the regional Chl-a outbreak observed in satellite imagery consistently occurs in late winter/early spring of most years, occasionally also in early autumn, but never in full winter or full summer time, it is likely representing the early spring and autumn phytoplankton bloom, controlled primarily by the increase in light availability in spring and replenishment of nutrients in autumn. The more intense offshore blooms recorded in March of 2006, 2009 and 2010 may result from late-winter and early-spring runoff in combination with short-term northerly winds over the shelf, a condition described by several authors (i.e. Guerreiro et al., 2013; Peliz and Fiúza., 1999; Ribeiro et al., 2005; Santos et al., 2004; Chapter 2). In situ measurements indicating enhanced productivity in the surroundings of Belatina Valley should, therefore, primarily reveal the presence of a front generated between the BP and the shelf-slope waters during a hydrologically and meteorologically highly transient period in this region (Guerreiro et al., 2013 – Chapter 2). Nevertheless, in view of the particular location,

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Chapter 3 other phenomena could be invoked to explain the local phytoplankton increase, which may be too short-lived and localized to be identified within monthly averaged Chl-a distribution maps. As suggested above, the abrupt seabed topography of the Nazaré Canyon is likely to induce perturbations in the flow of water masses on the shelf. Fronts between relatively productive coastal water masses and less-productive open ocean water masses will tend to meander across the canyon, adding complexity to spatial distribution of particulate matter in the surface water. Since the sampling cruise took place during the winter-spring transition when the water masses were still adjusting, the canyon topography might be expected to have a noticable influence on the circulation. In contrast, during typical summer-conditions, wind forcing will play a more prominent role in determining surface water circulation. Belatina Valley appears to be a region of significant topographic effect on the front of the low salinity BP, as indicated by the occurrence of the strongest vertical density gradients in this area. Quaresma (2012) reported on the existence of a barotropic water mass flux of convergent- divergent periodic motion between the interior of the canyon and the shelf close to Belatina Valley, driven by the barotropic onshore-offshore water flow. According to this author, the canyon axis acts as drain for shelf water at this location during every low tide. This water exchange may result in the concentration of nutrients within the surface water layer, whose time-integrated effect would result in a local nutrient-enrichment favorable for phytoplankton growth. Several modeling studies revealed the importance of ocean currents interacting with submarine canyons, enhancing productivity and influencing phytoplankton distribution by funneling and trapping plankton within the canyons. These studies highlight the predominant effect of local primary production on the canyon food web, in comparison to other potential sources (Bosley et al., 2004; Macquart-Moulin and Patriti, 1996; Skliris and Djenidi, 2006). In addition, one could speculate that internal tidal pumping driven by intensified vertical baroclinic oscillation around Belatina Valley could contribute to phytoplankton growth in this area, similar to what has recently been described from Monterey Canyon (California, USA) by Ryan et al. ( 2005; 2010). These authors described the upsurge of a wedge-shaped tongue of cold, dense water from the canyon, flowing up onto the continental shelf. The intruding water mass was observed to entrain a plume of nutrient-rich turbid water from the seafloor up to the surface, above which high concentrations of phytoplankton were observed. In the Nazaré Canyon, during a cruise performed in November 2002, a vertical turbid plume was observed at the Belatina Valley area, extending upward from a level of intense intermediate nepheloid layers at 800-900 m water depths to about 300 m. This plume was interpreted as reflecting resuspension by the canyon’s internal tide, enhanced by the strong density gradient between the ENACW (above) and the denser Mediterranean Outflow Water (MOW) (below) (Oliveira et al., 2007). Such baroclinic vertical oscillation, amplified in the canyon meander, may be responsible for bringing nutrients from below the canyon rim during winter, promoting phytoplankton growth in the upper part of the water column. However, our water column turbidity profiles and vertical distribution of coccolithophores and nutrients show no evidence of the occurrence of this process during the investigated late winter period, where enhanced nutrient concentrations appeared predominantly associated with the BP (see Guerreiro et al., 2013). Baroclinic activity

116 Influence of the Nazaré Canyon is more likely to gain in importance during stratified summer conditions.

3.5.3. Satellite data versus in situ measurements

Our observations, both long-term Chl-a concentrations obtained from satellite data and in situ quantification, suggest that the Nazaré Canyon may locally favor, at least indirectly, the development of phytoplankton, including coccolithophores. This is the case for the canyon head, which appears to be the stage of recurrent higher productivity in comparison to the adjacent shelf. However, in the case of Belatina Valley, where in situ observations revealed local Chl-a and coccolithophore cell enhancement, monthly averaged productivity obtained from satellite suggest that enhanced Chl-a production was not confined to that specific area but occurred over a much wider area including most of the shelf (transect B, Figure 11b). On the one hand, lacking in situ observations from outside the canyon, we cannot ascertain whether higher Chl-a and cell densities obtained from this area are actually confined to the canyon axis, or are part of a larger pattern not necessarily related to the canyon. On the other hand, it cannot be expected that monthly Chl-a averages obtained from satellite data will match exactly the coccolithophore and Chl-a peaks measured in situ and only representing one instant of the annual productivity. Different spatial and temporal scales are involved: whereas the satellite data reveal patterns of phytoplankton distribution at the surface at relatively high resolution, insight of phytoplankton productivity at deeper levels in the water column can only be obtained from in situ measurements. Differences between the two will expectedly be largest under the highly transient meteorological and oceanographic conditions characteristic of the late winter period, as prevailing during the cruise. Intensified baroclinic activity at Belatina Valley might well promote biological production events that are too deep and short-lived to be detected by monthly Chl-a averages obtained by satellite. The rapid response of certain species of coccolithophores to regional meteorological and hydrological variations off central Portugal was recently demonstrated by Guerreiro et al. (2013) (Chapter 2). Satellite imagery has a tremendous potential to describe larger-scale phenomena prevailing on the Portuguese margin, but it may not be the best approach to investigate smaller-scale processes, for which higher temporal and spatial resolution are probably required. Validation of hypotheses presented here requires additional sampling surveys integrated with meteorological and hydrological monitoring in order to address the seasonal and interannual variability of phytoplankton (in general) and coccolithophores (in particular), in relation with physical processes in the Nazaré Canyon.

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3.6. Conclusions

This study is the first attempt to characterize coccolithophore assemblages occurring in the context of an active submarine canyon. A late winter low-productive period was investigated in the Nazaré Canyon (off central Portugal) during which warm and saline waters fed by the IPC were still strongly influencing the hydrology of the shelf and slope, and the winter mixed layer occupied the entire water column of the shelf-upper slope. The canyon was clearly acting as a conduit for the onshore advection of relatively nutrient-poor oceanic waters to very nearshore areas (less than 10 km off the coast). Runoff prior and during the cruise was an important source of nutrients into the system, as indicated by high nutrient concentrations that were measured in the relatively low saline buoyant plume overlying the winter mixed layer in the coastal zone. Nevertheless, the weak correlation of nutrients with biomass suggests that phytoplankton production had not yet responded to higher nutrient availability, probably resulting from important advective mixing promoted by the BP during this period of intense runoff, sub-optimal light conditions due to cloud cover and initial relatively high suspended sediment load within the surface water layer (discussed in Guerreiro et al., 2013 – Chapter 2). Two main coccolithophore assemblages were distinguished, representing the gradient between the runoff-influenced coastal-neritic zone and the oceanic mixed water conditions that characterize the Portuguese margin during winter: (1) Emiliania huxleyi was the dominant taxon at the surface within more coastal-neritic conditions and, together with Gephyrocapsa ericsonii and Coronosphaera mediterranea, represent the more productive assemblage during the sampling period. (2) Syracosphaera spp. and Ophiaster spp. showed a clearly higher affinity for open-ocean conditions, displaying a generally broader vertical distribution. Closer to the coast, these taxa were able to compete well with E. huxleyi in the subsurface layer, suggesting that lower light and nutrient level within more neritic conditions were less limiting for Syracosphaera spp. and Ophiaster spp. as it was for E. huxleyi. Chl-a time series obtained from satellite data suggest that the Nazaré Canyon head is often the stage of high productivity between March and October, which makes the canyon head the most persistently productive part of the upper-middle canyon. In situ observations also revealed a coccolithophore diversity “hotspot” in this area, including both oligotrophic-oceanic and opportunistic-coastal taxa. The single occurrence of typically subtropical-oligotrophic species (i.e. Discosphaera tubifera, Palusphaera vandelii, Calcidiscus leptoporus) is interpreted as indicative for the shoreward flow of ENACWst intensified along the upper canyon during winter. In addition to these species, a diversified assemblage dominated by the productive E. huxleyi, G. ericsonii and C. mediterranea, together with other species which have their maximum occurrence in the canyon head area including both neritic/coastal (i.e. Gephyrocapsa oceanica, Acanthoica spp.) and neritic/oceanic species (i.e. Gephyrocapsa muellerae, Syracolithus dalmaticus, Alisphaera spp. and Michaelsarsia elegans) may also reflect exchange of water masses between neritic-coastal and oceanic regions through the canyon during winter. Local enhancement of nutrient concentration and coccolithophore cell concentration was

118 Influence of the Nazaré Canyon observed near the Belatina Valley, with E. huxleyi, G. ericsonii and C. mediterranea dominating the assemblage at the uppermost 25 m of the water column. In addition, monthly averaged satellite data reveal slightly higher Chl-a concentrations apparently roughly aligned with the canyon axis, close to Belatina Valley. We hypothesize that this imprint may be tracing the time- integrated effect of barotropic water mass flux into Belatina Valley and the meandering of the low-salinity front into this location. Based on our in situ observations and on recent studies identifying this narrower part of the canyon axis as an area of intensified vertical water movement, we suggest that Belatina Valley may potentially be a favourable region for phytoplankton local enhancement. Results presented here provide some valuable indications with regards to the important and persistet influence of the Nazaré Canyon on the ecology and distribution of coccolithophores and phytoplankton biomass at the central Portuguese margin. The results highlight the need of long-term multi-proxy investigations in order to address the seasonal and interannual variability in phytoplankton in relation with the seasonal- and/or topographically driven physical phenomena associated with the Nazaré Canyon.

Acknowledgements - This research was supported by the HERMIONE project (EC contract 226354) funded by the European Commission and the Cd Tox-CoN project (FCT-PTDC/MAR/102800/2008) funded by the Portuguese Science Foundation FCT. The first author benefits from an FCT PhD grant (FRH/BD/41330/2007). Filter samples were collected during the 2nd HERMIONE cruise of the Portuguese Hydrographic Institute (IH) on board of NRP Almirante Gago Coutinho. The authors are grateful to all the crew of the NRP Almirante Gago Coutinho and several researchers participating in the cruise for their valuable help during the collection of samples. A special thanks to the OC-IH CTD data acquisition team, João Vitorino, Manuel Marreiros, Inês Martins, Vânia Carvalho and Nuno Zacarias, and to Manuela Valença (QP-IH) for performing the compilation of nutrient data. All the samples were prepared and analyzed at NANOLAB, Geology Centre of Lisbon University (CEGUL). SEM observations were performed at the Institut de Ciències del Mar (ICM – CSIC, Barcelona, Spain). Constructive criticism and helpful suggestions from two anonymous reviewers are most gratefully acknowledged by the authors.

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Chapter 4

Coccoliths from recent sediments of the Central Portuguese Margin: taphonomical and ecological inferences

Chapter 4 Coccoliths from recent sediments of the Central Portuguese Margin: taphonomical and ecological inferences

Together with H. de Stigter, M. Cachão, A. Oliveira, A. Rodrigues. In revision, Marine Micropaleontology

Abstract

In this study we describe recent coccolith assemblages from surface sediments of the central Portuguese continental margin. Assemblages from the Nazaré and Lisbon-Setúbal submarine canyons are compared with those from adjacent shelf and slope regions. By investigating North-South and onshore-offshore trends in coccolith concentrations and species percentages, and by correlation with sediment characteristics (sediment bulk composition and particle-size, Corg/Ntot and sediment accumulation rate), (paleo)ecological information can be distinguished from taphonomical effects (dissolution, lateral transport and dilution with terrigenous material). Multivariate analysis was used to statistically reveal and summarize the most important signals preserved on the sedimentary record. Coronosphaera mediterranea, Helicosphaera carteri and Gephyrocapsa oceanica displayed a markedly coastal distribution, revealing to be good (paleo)ecological proxies for enhanced productivity in the upper Nazaré Canyon and Estremadura spur, whereas Calcidiscus leptoporus and the taxonomic group composed by Umbilicosphaera sibogae, Umbellosphaera irregularis and Rhabdosphaera spp. appeared to be a good proxy for production occurring further offshore and for onflow of ENACWst towards the southern part of the Portuguese shelf. Increase of Gephyrocapsa muellerae in the upper reaches of the Lisbon-Setúbal Canyon may be tracing the preferential onflow of oceanic temperate water masses (ENACWsp) through the canyon toward coastal regions, and/or indicating up-canyon transport of resuspended coccoliths in the benthic boundary layer. The mix of coccoliths from both coastal-neritic and oceanic species in the canyons appear to reflect their capacity to promote the exchange of water masses between more coastal and oceanic regions, in comparison to the adjacent shelf and slope regions, as well as the role of internal tides in disturbing and homogenizing the sedimentary record. Sediments from the Nazaré Canyon are clearly enriched in coccoliths from coastal-neritic species, suggesting a more dynamical and nutrient-rich environment favourable for r-selected species to develop, although some down-canyon displacement of coastal-neritic coccoliths should also be considered. On the contrary, relatively higher proportions of coccoliths from oceanic taxa in the

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Lisbon-Setúbal Canyon suggests more oceanic and stable conditions, probably in relation with its greater distance to the coastal dynamics and limited down-canyon transport. This study highlights the impact of sea bottom topography and related oceanographic circulation on both taphonomy and ecology of coccolithophores, and provides new insights in the role of submarine canyons in influencing the coccolithophore assemblages closer to the coast.

Key-words: coccoliths; (paleo)ecology; taphonomy; bottom dynamics; Nazaré and Lisbon- Setúbal canyons

4.1. Introduction

Calcareous nannoplankton, predominantly represented by coccolithophores, has the best fossil record of all marine phytoplankton, with the exception of polar regions (Ziveri et al., 2004). Their calcitic cell-covers (coccoliths or nannoliths sensu lato), are produced by biomineralization of tiny calcite crystals arranged according preferential orientations, and represent morphological elements with taxonomic and phylogenetic meaning (Pienaar, 1994; Young, 1994). By becoming preserved in the geological archive, the coccoliths store valuable information on palaeoenvironmental conditions from the photic zone (McIntyre and Bé, 1967; Roth, 1994; Baumann et al., 2000; Boeckel et al., 2008). As such they can be used as markers of paleoceanographic processes, sea surface water masses, productivity and climate change (e.g. Beaufort et al., 2001; 2011; Flores et al., 2000; Ziveri et al., 2004; Silva et al., 2008). The correspondence between the coccolith species assemblages preserved in the seabed and the living communities thriving in the adjacent photic layer is, however, complex, particularly within shallower marine environments such as continental shelves. Complexity further increases in heterogeneous and dynamic regions such as submarine canyons, often acting as morphological traps of sediment particles and organic matter from the continent and shelf, and simultaneously, as preferential conduits through which the transport of sediments between the coast and the deep sea is intensified (e.g. dense-water cascading and gravity-driven flow events) (e.g. Schmidt et al., 2001; Van Weering et al., 2002; Canals et al., 2006; Oliveira et al., 2007; De Stigter et al., 2007; 2011). Apart from their role in channeling water mass exchange and sediment transport between the shelf and slope, increased phytoplankton density has been reported to be associated to submarine canyons, resulting from upwelling and bottom sediment resuspension in the upper canyon reaches (e.g. Hickey, 1995; Kampf, 2006). The potential of physical processes within canyons to concentrate marine organisms in and around the canyons, also related to local enhancement of primary production, has been reported in several studies (e.g. Macquart-Moulin and Patriti, 1996; Bosley et al., 2004; Skliris and Djenidi, 2006). Whether any of this is reflected in recent fossil assemblages in canyon sediments is problematic, since high terrigenous

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Coccoliths from recent sediments sediment input and strong bottom dynamics typical of submarine canyons are expected to dilute and disturb the paleoecological signal. Here we report the results from a study of recent coccolith assemblages obtained from 92 surface sediment samples collected from the central Portuguese margin, where two major submarine canyons are located: the Nazaré Canyon and Lisbon-Setúbal Canyon. Little is known about the effect of physical processes operating in these canyons on the ecology of phytoplankton communities in the overlying water masses. Mendes et al. (2011) investigated the distribution and composition of phytoplankton assemblages in the Nazaré Canyon during an upwelling event, reporting the highest Chl-a concentrations occurring at the canyon head. According to these authors, persistently high concentrations of diatoms observed south of the canyon apparently reflect the occurrence of intensified upwelling along the southern rim of the canyon, extending its influence to the southern shelf, and persisting even during the period of relaxation of upwelling winds. The late-winter coccolithophore assemblage thriving in the Nazaré Canyon region was recently discussed by Guerreiro et al. (sumitted-a), who hypothesized the presence of local diversity and productivity “hotspots” related to the canyon’s topography. Emiliania huxleyi, Gephyrocapsa ericsonii, Coronosphaera mediterranea and Gephyrocapsa muellerae were the dominant species within the coccolithophore community. Gephyrocapsa oceanica was relatively more abundant at the canyon’s head and southern adjacent shelf, whereas Syracosphaera spp. and Ophiaster spp. were consistently thriving further offshore at the middle Nazaré Canyon. To reveal the (paleo)ecological information contained in calcareous nannoplankton assemblages from such a heterogeneous region as the central Portuguese margin, we applied multivariate analysis in this study, focusing on the larger and taphonomic-resistant coccolithophore species, and including data on sediment characteristics. Our aim is to contribute to the knowledge of this phytoplankton group, its distribution offshore central Portugal, and its potential as (paleo)ecological and (paleo)oceanographic proxy in the context of submarine canyons.

4.2. Regional setting

4.2.1. Central Portuguese margin

The central Portuguese margin has a relatively narrow shelf (20–50 km wide and a gradient of <1°), passing into a steep irregular slope (6–7°) below the shelf-break which is located at 160-200 m depth (Figure 4.1). The shelf is composed of thick Cenozoic detritical formations, filling structural basins formed during earlier rifting phases. The margin is dissected by a number of long submarine canyons, of which the Nazaré and Lisbon-Setúbal canyons are the most remarkable (e.g. Vanney and Mougenot, 1981; Mougenot, 1989; Alves et al., 2003). Surface sediments on the shelf are generally very coarse and sand-dominated, and include old littoral deposits formed during the Holocene transgression preserved at shallow water

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Chapter 4 depths. Finer-grained sediments generally increase with depth on the shelf, but also occur in muddy deposits located off the estuaries, in structural depressions at the middle shelf and in the canyons upper reaches. Fluvial discharge, coastal erosion and biogenic production are the main present day fine sediment sources (Dias, 1987; Van Weering et al., 2002; Oliveira et al., 2002). Further down in the continental slope, sediments change from slightly coarser and compositionally variable on the upper slope towards more uniform fine-grained and carbonate- richer hemipelagic muds on the deeper slope (De Stigter et al., 2007; 2011). Surface water circulation along the Portuguese margin is directly dependent on two major current systems that transport surface water masses from west to east across the Atlantic: the North Atlantic Current extending to the north of the Iberian Peninsula, and the Azores Current south of Iberia (Saunders, 1982; Pollard and Pu, 1985; Barton, 2001; Peliz et al., 2005). As the Azores Current flows eastwards, branches of this current smoothly loop northward into the Portugal Current and southward into the Canary Current (Saunders, 1982; Barton, 2001). Beneath the near-surface equatorward flow of the Portugal and Canary currents, the Iberian Poleward Current (IPC) can be recognized traveling poleward, counter to the general circulation and closely bound to the continental slope, its core extending about 300-400 m vertically. This current is mostly restricted to the subsurface layers along most of the eastern subtropical gyre, but it surfaces whenever the Trade Winds weaken or turn northward (Barton, 2001). Circulation over the Portuguese shelf and upper slope displays a marked seasonal variation associated with seasonal shifts in the position of the Azores high and Iceland low pressure systems (e.g. Haynes et al., 1993; Barton, 2001; Relvas et al., 2007). During summer, the Azores high migrates towards the central Atlantic, typically inducing Trade Winds to become northerly, inducing an equatorward circulation over the upper 150-200 m of the water column off Portugal. Under such conditions, the surface layer of about 30 m thick of relatively warmer and lighter water is swept offshore by Ekman transport, allowing colder, less salty and nutrient enriched subsurface water to rise to the surface along the coast (e.g. Fiúza, 1983; Haynes et al. 1993; Barton, 2001; Relvas et al., 2007; Alvarez et al., 2011). During winter, the Iceland low intensifies and the dominant wind regime becomes southerly along the western Portuguese margin. This induces the IPC to rise over the upper slope and shelf, where the poleward flow produces an onshore Ekman transport, in turn resulting in downwelling conditions over the shelf (Fiúza, 1983; Vitorino et al., 2002). River runoff is an important feature of the winter circulation over the western Portuguese margin. Important discharge particularly from the NW Portuguese rivers (Mondego, Douro, Minho, Lima, Vouga) results in the formation of low salinity water lenses in the coastal ocean (Peliz et al., 2005). The upper 500 m of water column off Portugal, including the surface mixed layer and the first thermocline, is constituted by the Eastern North Atlantic Central Water (ENACW). This water mass, representing the main source of the nutrient-rich upwelled waters on the Portuguese coast, shows considerable variation in its hydrological features as it travels along the coast (Fiúza, 1984; McCave and Hall, 2002). The ENACW has two main components of different origin, converging to this region: a lighter, relatively warm and salty subtropical branch (ENACWst) formed along the Azores Front, which gradually loses its characteristics as it

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Figure 4.1 - Geographical location of the central Portuguese margin. Black and green squares indicate location of multi- and boxcores analysed for, respectively, coccoliths and sediment characteristics. Squares with a black contour mark stations where sediment accumulation rate (SAR’s) was determined.

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Chapter 4 travels further northwards along the Iberian margin; a less saline colder water mass of subpolar origin (ENACWsp) slowly flowing southwards below the poleward subtropical branch, related with the Subpolar Mode Water formed in the eastern North Atlantic by winter cooling and deep convection (Fiúza et al., 1998). Underneath the ENACW a strong salinity gradient is noticed down to the core of the Mediterranean Outflow Water (MOW) lying at ~800–1400 m depths. The warmer and more saline MOW was observed interacting intermittently with the slope to acquire a weak turbidity of < 50 mg/m3 due to local resuspension caused by internal wave and slope current activity, contributing to load the overlying ENACW at 500–800 m (mixing zone between ENACW and MW) (McCave and Hall, 2002). The deeper water masses below the MOW comprise the Northeast Atlantic Deep Water (NEADW) below 2000 m, and the Lower Deep Water (LDW) at levels <4000 m (Van Aken 2000ab).

4.2.2. Submarine canyons

The Nazaré and Lisbon-Setúbal canyons are the largest submarine canyons of the central Portuguese margin, extending from near the shore to abyssal depth, and acting as preferential dispersal pathways of particulate matter and attached pollutants from the coast to the deep sea (De Stigter et al., 2007; 2011; Richter et al., 2009; Jesus et al., 2010; Martin et al., 2011) (Figure 4.1). The 211 km long Nazaré Canyon cuts across the full width of the Portuguese central margin, with its head located at ~50 m water depth and less than 1 km from the shore, and its mouth at almost 5 km water depth opening to the Iberian Abyssal plain. Its upper, middle and lower courses extend onto ~2000 m, ~4050 m and ~4970 m water depths, respectively (Lastras et al., 2009). The Nazaré Canyon is presently not connected to a major modern drainage system, and obtains its sediment input by capture of particles transported by littoral drift (Duarte et al., 2000) and along the shelf (Oliveira et al., 2007; De Stigter et al., 2007). Internal tidal currents actively resuspend and transport sediment in the upper and middle canyon, as reflected by high concentration of suspended particles in bottom waters, high horizontal and vertical sediment fluxes in the bottom water layer, and high sediment accumulation rates on the seabed (De Stigter et al., 2007). Intermittent sediment gravity flows transport fine-grained sediment further down to the lower canyon, but mass transport of coarser material by high-energy turbidity currents, dominant in shaping seabed morphology and sediment deposits of the lower canyon reaches (Arzola et al., 2008; Lastras et al., 2009) is rare at present. Resuspension of shelf sediments by winter storms and enhanced input of sediments by the flooding of rivers north and around the canyon head apparently contribute to trigger sediment gravity flows to the middle canyon (Oliveira et al., 2007; Martin et al., 2011; Masson et al., 2011). Residual currents above 300 m inside the canyon are well related with the wind regimes current in the western Portuguese margin: upwelling-favourable northerly winds over the shelf

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Coccoliths from recent sediments generate an onshore up-canyon flow, with upwelling occurring near the canyon head, whereas downwelling-favourable southerly winds lead the residual flow near or just above the canyon rim to become down-canyon. Below 300 m depth, the flow inside the canyon is mostly affected by the interaction of the northward flowing MOW with the canyon walls (Tyler et al., 2009). The Lisbon-Setúbal Canyon has a more complex morphology, fed by two main branches: the E-W oriented Setúbal branch and the N-S trending Lisbon branch. Like the Nazaré Canyon, the latter is deeply incised into the continental shelf and slope, and extends down to the abyssal plain at depths >4800 m. Different from the Nazaré Canyon, however, the Lisbon-Setúbal Canyon heads, located in somewhat deeper water a few km off the coast, are connected with two major river systems, i.e. Tagus and Sado rivers. The Lisbon and Setúbal branches merge at 2010 m depth, from there the middle course is measured down to the canyon mouth at 4170 m water depth, and the lower course extends down to the edge of the Tagus abyssal plain, at ~4860 m depth (Lastras et al., 2009). Recent findings of De Stigter et al. (2011) indicate that the Lisbon Setúbal-Canyon is presently nearly inactive in terms of down-canyon sediment transport, probably due to the presence of an overall up-canyon direction of net water transport, leading the particles to settle in the upper canyon towards the canyon head rather than disperse them down-canyon, and the apparent rareness of sediment gravity flows, which in other canyon systems (e.g. Nazaré Canyon) are the dominant mechanism of down-canyon dispersal. Fine-grained predominantly lithogenic particles from the adjacent shelf areas accumulate in their upper reaches, whereas the sediment deposited further down in the middle and lower canyon reaches is essentially hemipelagic, similar to the sediment found on the adjacent continental slope.

4.3. Material and methods

4.3.1. Cruises and surface sediment sampling

Surface sediment cores used in this study were recovered during several cruises with RV Pelagia of Royal NIOZ, held in November 2002, October 2003, April/May 2004, May 2005, September 2006 and March 2011 in the central Portuguese margin (cruises 64PE204, 64PE218, 64PE225, 64PE236, 64PE252 and 64PE332, respectively). Coring equipment and methodology are described in De Stigter et al. (2007, 2011). Sediment coring was concentrated on six transects crossing the central Portuguese margin in an approximately E-W direction: (1) three transects covering the Nazaré, Lisbon-Setúbal and Cascais canyons; (2) three transects across the shelf and open slope off Cape Mondego, Estremadura spur and off Cape Sines. Coring positions are shown in Figure 4.1 and listed in the Appendix D.

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4.3.2. Laboratory and microscope analysis

4.3.2.1. Sedimentological analysis

Sedimentological data presented in this paper have been previously presented and discussed by De Stigter et al. (2007, 2011), Jesus et al. (2010) and Costa et al. (2011), with the exception of material from Stations PE252-01 to -07 on the shelf and slope region west of Cape Mondego, and Stations PE252-40, PE252-43 to -46 and PE252-49 in the Nazaré Canyon and on the adjacent middle shelf. Analytical methodology for determining lithogenic material, carbonate and organic matter content, particle-size, and sediment accumulation rates, also used for analysis of additional cores from stations mentioned above, is described in De Stigter et al. (2007, 2011).

4.3.2.2. Calcareous nannoplankton

Calcareous nannoplankton was studied from freeze-dried sediment samples from the top 0.5 or 1 cm of the collected box- and multicores. Slides were prepared following the random settling procedure (Flores and Sierro, 1997) and observed under optical polarizing microscope (Olympus BX-40), at 1250× magnification. For coccolith species ≥ 3µm, a minimum of 300 individual coccoliths, or nannoliths s.l. (here abbreviated to “nanno”) was counted and identified in each slide to determine the species abundances (nanno/g). Florisphaera profunda and small placolith taxa Emiliania huxleyi and Gephyrocapsa ericsonii were counted separately, for which approximately ten vision fields were counted to estimate the coccolith concentrations of these species. Concentrations were determined according to the following equation:

V Pa 1 (1) N  n    Vp Oa W

Where, N = nanno/g, n = number of counted coccoliths, V = volume within the glass bottle (10000 µl), Vp = volume pipetted and injected into the Petri dish, Pa = Petri dish area, Oa = observed area (obtained by the number of vision fields, VF, at the microscope, multiplied by the unit area correspondent to the microscope; 1 VF Olympus BX-40 = 0.02 mm2), and W = weight of the sediment sample. The number of coccoliths per gram of sediment will be generally termed as “coccolith concentration” throughout the text, to distinguish from the “relative abundances” calculated as % relative to total coccoliths. To magnify the more robust and larger sized coccolith species and minimize possible bias by differential dissolution, small placolith taxa Emiliania huxleyi and Gephyrocapsa ericsonii were ruled out from the (paleo)ecological analysis, and used as a general qualitative indicator for the degree of preservation of the observed coccolith assemblages. F. profunda was also excluded from the analysis due to difficulties in its identification within highly terrigenous sediment samples as those collected from the studied shelf-slope region.

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Coccoliths from recent sediments

Nine taxa of coccolithophores were selected for this (paleo)ecological study: Calcidiscus leptoporus (Cl), Coccolithus pelagicus s.l. (Cp), Coronosphaera mediterranea (Cm), Gephyrocapsa muellerae (Gm), Gephyrocapsa oceanica (Go), Helicosphaera carteri (Hc), Umbilicosphaera sibogae, Umbellosphaera irregularis and Rhabdosphaera spp. Due to their scarcity and the fact that all the three latter taxa are considered as tracers for the onflow of oceanic warmer currents driven along the Azores current onto the Portuguese shelf (Cachão et al., 2000) they were grouped into one single taxonomic variable (UUR). Relative abundances (%) were determined relative to the sum of the seven taxonomic groups (≥ 3 µm).

4.3.3. Statistical analysis

A Spearman correlation coefficient matrix was built upon a data matrix with the coccolith taxa percentages and depth, distance to coast, total coccoliths per gram, percentage of CaCO3, lithogenic material and organic matter, sediment accumulation rate (SAR), median particle-size, and percentage of coccoliths with sizes >6 µm, between 5 and 6 µm , and between 5 and 3 µm (52 cases). A default p-level of 0.05 was considered. Coccolith size classes were defined on the basis of coccolith morphometric measurements earlier performed by Cros (2001) and Narciso et al. (2006), such that: size class >6 µm includes the coccolith concentrations of Calcidiscus leptoporus, Coccolithus pelagicus and Helicosphaera carteri; size class between 5 and 6 µm includes the coccolith concentrations of Gephyrocapsa oceanica and Umbilicosphaera sibogae; and finally, size class between 3 and 5 µm includes the coccolith concentrations of Coronosphaera mediterranea and Gephyrocapsa muellerae. A statistical multivariate analysis (r-mode Factor Analysis by Statistica 10) was performed upon a data matrix with the coccolith taxa percentages and the above-mentioned environmental variables, and in addition modal sediment particle-size (µm) and molar Corg/Ntot ratio, but excluding total coccoliths per gram, SAR and the three size classes of coccoliths (63 cases). Results from the original data matrix were optimized through Varimax Raw rotation.

4.4. Results

4.4.1. Sedimentary cover in the submarine canyons and adjacent shelf and slope

Characteristics of superficial sediments from the submarine canyons and adjacent shelf and slopes of Estremadura spur and west of Cape Sines were previously presented by De Stigter et al. (2007, 2011), Jesus et al. (2010) and Costa et al. (2011), revealing that sediments from the canyons significantly differ from those of their adjacent continental margins. The most striking sedimentological features evidenced in Figure 4.2 concern the differences between the canyons upper reaches and their adjacent coastal regions. Much finer- grained sediments and higher percentages of lithogenic material and organic matter are recorded from the canyons, whereas a relatively more uniform distribution of particle-size is also

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Chapter 4 recorded along their axis, particularly in the Nazaré Canyon. The canyon seabed and lower walls were observed to be covered by a superficial layer of mud predominantly composed of lithogenic material which, in the case of Nazaré Canyon, extends downwards to its lower section (De Stigter et al., 2007). Adjacent to the canyons, the sedimentary cover is much coarser near the coast, particularly off Cape Mondego, and abruptly changing into fine-grained sediments in the shelf-slope transition. Higher percentages of carbonates and lower percentages of organic matter are also noticed in coastal areas adjacent to the canyons (Figure 4.2a-e and

Table 4.1). Higher molar Corg/Ntot ratios in the canyons indicate a markedly terrestrial origin of the organic matter in these regions (Middelburg and Nieuwenhuize, 1998; Alt-Epping et al., 2007) (Figure 4.2e). Highest SAR’s in the upper and middle canyon reaches (Figure 4.2f) reflect their role as morphological traps and temporary depositories of particles in transit along the shelf (De Stigter et al., 2007; 2011). The highest SAR’s, molar Corg/Ntot ratios and percentage of lithogenic and organic material, were found in the upper reaches of the Nazaré Canyon. On the contrary, lower SAR’s were determined for the canyon edges and adjacent margin areas. The lowest SAR’s obtained from offshore areas, in the lower canyon reaches and adjacent slope areas are most likely overestimated as bioturbation was not taken into account in calculation of SAR’s from down-core radio-isotope profiles (De Stigter et al., 2007, 2011). For this reason, higher SAR’s from the open slope of Estremadura spur should be carefully considered. Low terrigenous input arriving to this region, as testified by the extensive areas of rock outcrops, is possibly due to relatively large distance from continent and bypassing of lithogenic sediment through canyons north and south of Estremadura Spur (Jesus, 2011). The Estremadura spur and region west of Cape Sines reveal slightly coarser sediment particle-size and variable composition on the upper slope, changing towards more uniform fine- grained hemipelagic muds on the deeper slope. Towards the coast sediments off Sines become coarser. In terms of bulk composition, sediments off Sines are remarkably uniform with water depth and similar to those from the Setúbal and Cascais canyons, whereas the Estremadura slope reveals distinctively lower lithogenic and higher carbonate content (De Stigter et al., 2011; Jesus, 2011). The coarsest sediments of the entire study area were recorded on the shelf and upper slope west of Cape Mondego. On the shelf, sediments have slightly higher lithogenic and lower carbonate and organic matter content than at comparable depths off Sines. At slope depths, sediments off Mondego have similar Corg/Ntot, particle-size and compositional features as those from the other slope regions, with lithogenic and carbonate percentages somewhat in between those of the Estremadura and Sines slopes. The shelf-slope transition is characterized by a noticeable change of the seabed sedimentological features, with the slope recording relatively higher percentages of carbonates and organic matter.

Lower molar Corg/Ntot ratios outside the canyons indicate a generally more marine signature of the sediment organic matter in these regions.

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4.4.2. Calcareous nannoplankton

A total of 18 distinct coccolith taxa were recognized using polarizing light microscopy, of which only 9 taxa (= 7 taxonomic groups) were selected for this (paleo)ecological study, based on their relatively higher coccolith concentrations and coccolith dimension (≥3 µm) and robustness (see section 3.3.2). Small placolith taxa Emiliania huxleyi and Gephyrocapsa ericsonii were ruled out of the species percentage determinations, whereas their estimated coccolith concentrations are here presented as a general indicator of the degree of preservation of the coccolith assemblage. The complete list of the observed taxa is presented in Appendix A.

4.4.2.1. Coccolith concentrations

Total coccolith concentrations of species ≥3 µm varied between 3×106 nanno/g at the shelf of Estremadura Spur and 3×109 nanno/g at the lower slope off Cape Mondego, with an average abundance of 9×108 nanno/g. Gephyrocapsa muellerae was the most abundant species, followed by Calcidiscus leptoporus, Gephyrocapsa oceanica, the taxonomic group composed by Umbilicosphaera sibogae, Umbellosphaera irregularis and Rhabdosphaera spp. (UUR), Coronosphaera mediterranea, Coccolithus pelagicus and Helicosphaera carteri. Mean and maximum coccolith concentrations of each species at the five sectors are indicated in Table 4.1. Coccolith concentrations generally decrease towards the coast, except in the upper reaches of the canyons where important values are noticed (Figure 4.3a). High concentrations were clearly more associated to finer-grained and carbonate-richer sediments further offshore, as indicated by the strong negative correlation with sediment particle-size (r2 = -0.83) (Figure 2 4.3b and Table 4.2) and positive correlation with percentage of CaCO3 (r = 0.50) bottom depth (r2 = 0.64) and distance off the coast (r2 = 0.56) (see Table 4.2). All the taxonomical groups show this distribution trend, particularly clear in the case of C. pelagicus, G. muellerae, G. oceanica and UUR. C. mediterranea and H. carteri reveal a more irregular W-E distribution, with higher abundances found at intermediate distances to the coast (~ between 90-110 and 50 km off the coast), and recording high abundances in the Nazaré Canyon. C. leptoporus has a more consistently oceanic distribution, even within the canyons (data not shown; Guerreiro et al., submitted-c; Chapter 5). Total coccolith concentrations of small placolith species ranged between 2×106 and 2×109 nanno/g (average 4×108 nanno/g) for belonging to Emiliania huxleyi, and between 4×105 and 2×109 nanno/g (average 5×108 nanno/g) for Gephyrocapsa ericsonii. Mean and maximum coccolith concentrations of the two species at the five sectors are indicated in Table 4.1. In terms of concentrations, these two species showed a distribution pattern similar to that of larger coccolith species (data not shown).

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Table 4.1 – Mean and maximum coccolith abundances, relative to sediment dry weight and relative to the sum of common coccoliths ≥ 3 µm, of the seven selected taxonomic groups along the five investigated transects. Minimum and maximum values of total coccolith abundance (nanno/g), CaCO3 (weight %), organic material (weight %), 2 lithogenic fraction (weight %), molar Corg/Ntot ratio, modal and median particle-size (µm), and sediment accumulation rates (SAR g/cm /yr) are also indicated.

Taxa Mondego transect Nazaré canyon Estremadura spur Lisbon-Setúbal canyon Sines transect nanno/g mean max. mean max. mean max. mean max. mean max. Calcidiscus leptoporus 1.8×108 5.9×108 4.2×107 3.4×108 1.1×108 5.9×108 7.5×107 2.2×108 1.1×108 2.9×108 Coronosphaera mediterranea 3.2×107 9.5×107 3.3×107 7.6×107 2.3×107 8.9×107 5.4×107 1.4×108 7.0×107 1.2×108 Coccolithus pelagicus 2.4×107 7.8×107 1.2×107 3.4×107 9.9×106 4.8×107 2.4×107 6.0×107 1.7×107 3.3×107 Gephyrocapsa muellerae 7.6×108 2.1×109 3.1×108 1.5×109 5.8×108 1.7×109 6.6×108 2.1×109 9.6×108 1.9×109 Gephyrocapsa oceanica 1.1×108 3.2×108 7.4×107 1.5×108 5.4×107 1.5×108 1.6×108 3.5×108 1.3×108 2.4×108 Helicosphaera carteri 2.4×107 7.7×107 2.4×107 5.3×107 2.0×107 7.6×107 3.0×107 8.7×107 2.7×107 8.7×107 UUR 5.7×107 5.7×107 1.4×107 6.5×107 3.3×107 1.1×108 4.1×107 1.4×108 7.9×107 2.1×108 Emiliania huxleyi (< 3µm) 5.5×108 1.7×109 2.4×108 8.4×108 3.5×108 1.5×109 4.9×108 1.1×109 6.8×108 1.3×109 Gephyrocapsa ericsonii (< 3µm) 5.4×108 2.0×109 1.9×108 6.6×108 4.0×108 1.4×109 5.0×108 1.2×109 1.1×109 1.8×109 % mean max. mean max. mean max. mean max. mean max. Calcidiscus leptoporus 9 19 5 30 9 24 6 22 2 5 Coronosphaera mediterranea 4 7 9 27 4 6 6 10 3 10 Coccolithus pelagicus 2 4 3 5 2 5 2 5 8 11 Gephyrocapsa muellerae 65 79 55 78 55 76 62 79 11 20 Gephyrocapsa oceanica 13 28 19 31 22 66 18 42 65 77 Helicosphaera carteri 4 7 6 14 4 9 3 6 5 10 UUR 3 8 2 6 4 12 3 9 5 8 Total coccoliths ≥ 3µm (nanno/g) 1.2×109 3.3×109 5.1×108 2.2×109 8.3×108 2.8×109 1.0×109 3.1×109 1.4×109 2.9×109

CaCO3 (wt %) 29 49 14 33 41 60 21 29 27 41 OM (wt %) 1 2 4 6 1.7 2.3 3 5 2 3 Lithogenic (wt %) 70 94 82 89 57 67 76 87 71 75

Corg/Ntot 7.9 9.4 12.2 43.7 7.9 8.3 8.6 10.2 8.2 9.1 Mode (µm) 119 390 26 97 31 185 21 140 30 169 Median (µm) 92 328 17 87 16 77 17 128 21 140 SAR (g/cm2/yr) 0.09 0.26 0.59 4.59 0.10 0.29 0.15 0.56 0.05 0.11

Coccoliths from recent sediments

Figure 4.2 – General characteristics of surface sediments: (a) median particle size (µm) (b), (c) and (d): percentage of, respectively, lithogenic material, organic matter and carbonates; (e): molar Corg/Ntot ratios, 2 (f): sediment accumulation rate, SAR (g/cm /yr). Outlier 225-39mc1 with molar Corg/Ntot of 44 is indicated by an arrow pointing up.

In addition to the coccoliths, 25 intact coccosheres were also observed in the investigated sediment samples. The more common species were G. oceanica and G. muellerae, but also G. ericsonii, C. pelagicus, Braarudosphaera bigelowi and Rhabdosphaera spp. Most of the coccospheres were found in samples from the submarine canyons, particularly the Lisbon- Setúbal Canyon, at water depths between 179 and 3914 m.

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Figure 4.3 – Total coccolith abundances relative to dry sediment weight (nanno/g), plotted against distance to coast and median particle size.

4.4.2.2. Coccolith species percentages

In terms of relative abundance within the group of common larger coccoliths (i.e. excluding small placolith species Emilinia huxleyi and Gephyrocapsa ericsonii), G. muellerae largely dominates the assemblage in all the studied sectors, at all depths, showing percentages between 60 % and 80 % further offshore. Nearer to shore, where relative abundances are lower overall except in the Lisbon-Setúbal Canyons, the lowest percentages dropping below 40 % occur on the Estremadura shelf. Whereas in the upper reaches of the Nazaré Canyon G. muellerae recorded relatively lower percentages similar as in the adjacent coastal regions, this species revealed distinctly higher abundances in the upper reaches of the Lisbon-Setúbal Canyon, similar to those from further offshore. No correlation was obtained between this species percentages and sediment particle-size in the study area, except off Cape Sines where a negative correlation is noticed (r2 = 0.46) (Figure 4.4d). Gephyrocapsa oceanica, the second most abundant species, shows a clearly coastal preference in its distribution, with highest relative abundance around 60 % on the Estremadura shelf (see the plot on the left side of Figure 4.4e). G. oceanica clearly decreases in offshore direction to abundances around 10 %. A basically similar distribution pattern is observed in the canyons, whereas the lowest percentages close to the coast were recorded in the Lisbon-Setúbal Canyon. Low correlation was obtained between this species percentages and sediment particle- size in the canyons and Estremadura open slope (r2 < 0.15), whereas a positive correlation is noticed off Cape Mondego and Cape Sines (r2 = 0.73 and r2 = 0.45, respectively) (Figure 4.4e). Coronosphaera mediterranea and Helicosphaera carteri are also generally more abundant closer to shore, the first species reaching particularly high abundances up to 20-25 % in the upper Nazaré Canyon. Further offshore, the abundance of both species decreases to less than 5 %. Although with considerable variation, abundance of H. carteri in the Nazaré Canyon follows a pattern more similar to that from the adjacent shelf and slope. Abundances in the Lisbon-Setúbal Canyon are consistently lower, however. No significant correlation was found between C. mediterranea and sediment particle-size (r2 < 0.2), whereas H. carteri reveals a

136 Coccoliths from recent sediments clearly positive correlation off Cape Mondego (r2 = 0.65) and Cape Sines (r2 = 0.75) (Figures 4.4b and f). Calcidiscus leptoporus is consistently more abundant further offshore, particularly on the Estremadura spur and west of Cape Mondego (Figure 4.4a). Closer to shore, relative abundances are less than 5 %, except in the southern part of the study area in the Lisbon-Setúbal Canyon and Sines shelf where higher abundances are found. Relative abundances in the canyons tend to be higher, but show a similar increase in offshore direction. C. leptoporus reveals no correlation with sediment particle-size in the study area, except off Cape Mondego where a negative correlation is noticed (r2 = 0.55). UUR are consistently better represented at intermediate distance to shore, generally coinciding with upper slope depths. A similar pattern is visible in the canyons. This taxonomic group reveals a weak negative correlation with particle-size at the Lisbon-Setúbal Canyon (r2 = 0.28) and off Cape Sines (r2 = 0.39) (Figure 4.4g). C. pelagicus, the least abundant species of those considered, with abundances generally below 5%, revealed the weakest coast-ocean gradient in the study area, although this species is generally better represented nearer to shore, in the upper canyon reaches and the adjacent shelf areas. No significant correlation was obtained between this species percentages and sediment particle-size, although a positive correlation is noticed off Cape Sines (r2 = 0.86) (Figure 4.4c). All the taxa revealed a higher variability of relative abundances in the Nazaré Canyon, i.e. both low and high percentages were determined at both shorter and greater distances of the coast, particularly from sediments with median particle-sizes between 7 and 20 µm. Whereas G. oceanica and C. leptoporus display a rather clear oceanic-coastal gradient at both submarine canyons and adjacent regions (increasing and decreasing gradients, respectively), other species such as C. mediterranea, H. carteri and G. muellerae display different tendencies in and outside the upper canyon reaches. G. muellerae generally decreases towards the coast outside the canyons, whereas important percentage values of this species are recorded in the Lisbon-Setúbal Canyon. C. mediterranea stands out for recording much higher values in the upper canyon sections, particularly in the Nazaré Canyon, in comparison to the adjacent shelf for comparable distances to the coast. Likewise, H. carteri recorded its highest percentages in the Nazaré Canyon whereas the Lisbon-Setúbal Canyon and Estremadura spur recorded its lowest percentage values close to the coast. Spearman correlation coefficients generally confirm the distributions described above. Significant positive correlations are found between individual coastal-neritic taxa as well as between individual oceanic taxa, and negative correlations between coastal and oceanic taxa. Each group is clearly associated to a specific environmental setting: the oceanic group is often positively correlated with “oceanic factors” such as bottom depth, distance to coast, total coccoliths per gram and carbonates, whereas the coastal-neritic group is often positively correlated with “continental factors” such as coarser sediment particle-size, lithogenic material and high Corg/Ntot ratio (Table 4.2).

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Figure 4 –Coccolith relative abundances (%) plotted against distance to coast and median particle-size: Calcidiscus leptoporus (a), Coronosphaera mediterranea (b), Coccolithus pelagicus (c), Gephyrocapsa muellerae (d), Gephyrocapsa oceanica (e), Helicosphaera carteri (f) and Umbilicosphaera sibogae, Umbellosphaera irregularis, Rhabdosphaera spp. (UUR) (g). It should be noted that only the samples for which sedimentological data are available were considered in these plots (i.e. stations from the shelf at Estremadura Spur are not represented).

Three size classes of coccoliths, i.e. liths 3-5µm, 5-6 µm and > 6 µm, were also included in the correlation matrix, to assess possible selective transport according to size. No significant correlation was found between different coccolith size classes and sediment particle-size (Table 4.2).

138 Coccoliths from recent sediments

Figure 4 (Cont.)

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Table 4.2 - Spearman correlation coefficient matrix showing the relationships between the relative abundance of coccolith taxa and depth, distance to coast, total coccoliths per gram dry sediment, percentage of CaCO3, lithogenic material and organic matter, sediment accumulation rate (SAR), median particle-size (P-S), and percentage of coccoliths with sizes >6 µm, between 5 and 6 µm, and between 3 and 5 µm. Only the significant correlations are presented (≥0.45), with the highest highlighted (0.7 = light brown; ≥0.8 = dark brown). Default p-level of 0.05.

Depth Distance Coccoliths Cp Hc Cl Go Gm Cm UUR CaCO3 OM Lithos SAR P-S Liths >6 µm Liths 5-6 µm Liths 3-5 µm m km nanno/g % % % % % % % % % % g/cm2/yr µm % % % - - Depth 1 0.72 0.64 -0.45 0.73 0.50 -0.66 0.47 -0.56 0.60 0.48 - - Distance 0.72 1 0.56 0.72 0.59 0.56 -0.54 -0.50 -0.52 -0.72 0.75 0.59 - - Coccoliths 0.64 0.56 1 -0.65 0.69 0.63 0.50 -0.52 -0.83 -0.56 0.62 0.47 Cp 1 0.51 -0.52

- Hc -0.45 -0.65 1 0.63 -0.63 0.50 -0.56 0.59 0.59 -0.59 0.51 - - Cl 0.73 0.72 0.69 -0.51 1 0.60 0.66 -0.66 -0.58 0.64 -0.63 0.67 0.64 - Go -0.60 -0.75 -0.62 0.63 1 -0.81 0.73 -0.61 -0.59 0.58 0.50 0.99 -0.74 0.67 - - Gm -0.63 1 -0.81 0.94 0.81 0.64 - Cm -0.48 -0.59 -0.47 0.50 0.73 -0.64 1 0.55 0.72 0.64 - UUR 0.50 0.59 0.63 -0.56 0.60 1 0.59 -0.59 -0.46 -0.55 -0.51 0.61 - CaCO 0.56 0.50 0.66 0.59 1 -0.62 -0.99 -0.55 3 0.59 OM 0.55 -0.62 1 0.57 0.49

- Lithos -0.54 -0.52 0.58 -0.59 -0.99 0.57 1 0.53 0.66 SAR -0.50 -0.46 0.49 1 0.46

- P-S -0.66 -0.52 -0.83 0.59 0.50 -0.55 1 0.58 Liths >6 µm 0.47 0.51 0.64 1

- Liths 5-6 µm -0.56 -0.72 -0.56 0.59 0.99 -0.81 0.72 -0.51 -0.55 0.53 0.46 1 -0.75 0.63 - - Liths 3-5 µm -0.59 0.94 -0.75 1 0.52 0.74

Coccoliths from recent sediments

4.4.3. Multivariate statistical analysis

Results from factor analysis revealed four distinct factor assemblages explaining 70 % of the total variance in the data (Table 4.3). Factor 1 (F1) explains 38 % of total variability, with C. leptoporus (Cl), water depth and distance to coast recording the highest (negative) factor loadings, in opposition to C. mediterranea (Cm) and G. oceanica (Go) (positive loadings). Factor 2 (F2) explains 16 % of total variance and it is represented by sediment particle-size (positive loadings) in opposition to organic matter (OM) (negative loadings). Factor 3 (F3) explains 9 % of total variance and it is represented by H. carteri (Hc), Cm, Go (C. pelagicus – Cp, and OM) (positive loadings) in opposition to G. muellerae (Gm) (negative loadings). Factor

4 (F4) explains 7 % of total variability and it is represented by CaCO3 and UUR (positive loadings) in opposition to Litho, OM and molar Corg/Ntot ratios (negative loadings). Samples with F1 positive scores (influenced by the variable cluster Cm and Go) are better represented closer to the coastline in all the investigated sectors, particularly in the upper reaches of the submarine canyons. Samples with F1 negative scores (influenced by the variable cluster Cl, depth and distance to coast) are clearly better represented further offshore. The two samples from the lowermost Nazaré Canyon show conspicuously diverging scores on F1 (Figure 4.5a). Samples with F2 positive scores (represented by coarser sediment particle-size) are better represented closer to the coastline, on the shelves off Cape Mondego and Cape Sines. Lack of sedimentological data from the shelf at Estremadura spur does not allow a comparison for this area. Samples with F2 negative scores (represented by OM) are generally better represented further offshore on the open slope areas, whereas the canyons and especially Nazaré Canyon typically show negative scores on F2 along their entire length (Figure 4.5b). Samples with the highest F3 positive scores (represented by the variable cluster Hc, Cm, Go, Cp and OM) appear concentrated relatively close to the coast in the upper Nazaré Canyon, whereas lower scores without a clear longitudinal or latitudinal separation of positive and negative scores is observed in the remaining areas. Samples with F3 negative scores (represented by Gm) are preferentially distributed further offshore, except in the upper canyon reaches, where this factor becomes more important close to the shore, particularly in the Lisbon- Setúbal Canyon (Figure 4.5c). The distribution of F4 seems to be dominated by the contrast between carbonate-rich pelagic sediments characterized by low OM content of marine signature, versus more lithogenic-rich sediments characterized by relatively higher OM content with a terrigenous signature. Samples with F4 positive scores (represented by the variable cluster CaCO3 and UUR) prevail on the Estremadura slope. Samples with F4 negative scores (represented by Litho,

OM and molar Corg/Ntot) are better represented along the canyons (Figure 4.5d).

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Table 4.3 - Results from factor analysis: factor loadings, eigenvalues and percentage of the explained variance obtained for the investigated surface sediment samples (r-mode Factor Analysis by Statistica 10; highlighted loadings are > 0.5). The variables included in the analysis were: coccolith species percentages (Cl – Calcidiscus leptoporus; Cm – Coronosphaera mediterranea; Cp – Coccolithus pelagicus; Gm – Gephyrocapsa muellerae; Go – Gephyrocapsa oceanica; Hc – Helicosphaera carteri; UUR - Umbilicosphaera sibogae, Umbellosphaera irregularis, Rhabdosphaera spp.); water depth (m); distance to coast (km); percentage of organic matter (OM), carbonates (CaCO3) and lithogenic fractions (Litho); molar Corg/Ntot ratios; modal and median particle sizes (P-S, µm).

Factor 1 Factor 2 Factor 3 Factor 4

Cl -0.88 -0.06 -0.03 0.26 Cm 0.48 -0.26 0.67 -0.14

Cp -0.19 0.21 0.39 -0.25 Gm -0.03 -0.01 -0.94 0.15 Go 0.47 0.17 0.65 -0.34 Hc 0.29 0.29 0.68 -0.23 UUR -0.30 -0.24 -0.32 0.44 Depth -0.82 -0.25 -0.23 0.04 Distance -0.74 -0.09 -0.29 0.31

CaCO3 -0.20 0.14 -0.20 0.91 OM 0.21 -0.51 0.37 -0.46 Litho 0.19 -0.08 0.17 -0.90

Corg/Ntot 0.08 0.12 -0.03 -0.40 Median P-S 0.19 0.89 0.04 0.00 Modal P-S 0.11 0.87 0.09 0.17 Eigenvalue 5.6 2.4 1.3 1.1 Total var. (%) 37.6 16.2 8.9 7.4

4.5. Discussion

4.5.1. General bottom conditions of the study area

The central Portuguese margin is a highly heterogeneous region, both topographically and in terms of sedimentary cover. The most striking expression of this heterogeneity are the two major submarine canyons, Nazaré and Lisbon-Setúbal canyons, which by cutting across the continental shelf and slope disturb the prevailing pattern of sediment distribution parallel to the isobaths on the shelf and slope. Highest sediment accumulation rate, lithogenic and organic matter content and molar

Corg/Ntot ratios in the upper Nazaré Canyon clearly indicate that this area is presently acting as a sediment depocenter within the central Portuguese margin, actively capturing material of continental origin (Epping et al., 2002; Oliveira et al., 2007; De Stigter et al., 2007) (Figure 4.2). The massive occurrence of nepheloid layers in the upper part of the Nazaré Canyon, and the very high sediment fluxes to the canyon floor as recorded in sediment traps and in seabed deposits, are clear evidence of the present-day activity of this canyon (De Stigter et al., 2007;

142 Coccoliths from recent sediments

Figure 4.5 - Factor scores obtained from the data matrix, plotted against distance to coast: factor 1 (a), factor 2 (b), factor 3 (c) and factor 4 (d). Species/variables ordered in sequence of decreasing positive factor loadings (in brackets those with less importance), and after / increasing negative loadings. For complete taxonomic references see Table 4.3.

Oliveira et al., 2007). Although the Nazaré Canyon head is not presently connected to a major drainage system, it is located very close to the coastline (i.e. ~50m water depth; Lastras et al., 2009) favouring sediment input by capture of particles transported by littoral drift (Duarte et al., 2000) and along the shelf (De Stigter et al., 2007; Oliveira et al., 2007). Relative homogeneity in composition and texture of bottom sediments along the Nazaré Canyon axis reflects the active transport of particulate matter along this canyon system (De Stigter et al., 2007). Intermittent down-canyon sediment gravity flows were observed redistributing sediments along the entire length of the Nazaré Canyon axis (De Stigter et al., 2007; Martin et al., 2011).

Relatively lower sediment accumulation rate, organic matter content and molar Corg/Ntot ratios in the Lisbon-Setúbal Canyon suggest a lesser sedimentary contribution from the continent in comparison to the Nazaré Canyon (Figure 4.2). Although the Lisbon-Setúbal Canyon is connected with two major river basins (i.e. Tagus and Sado rivers), the more distant position of the canyon heads relative to the coastline results in a sedimentary regime that is less affected by dynamic coastal processes. Although this canyon is effectively trapping sediment in its upper reaches, the sediment appears to be mostly derived from vertical flux (De Stigter et al., 2011). A markedly different and more heterogeneous sedimentary signature was recorded in the regions adjacent to the canyons. Coarse sediment prevailing on the inner shelf reflects the effect of present-day winnowing by waves and currents in the coastal zone, whereas coarse deposits further offshore were formed during stages of lower sea level in the past. Finer grained

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Chapter 4 sediments are progressively sorted as they are transported from shallower towards deeper areas. Much lower sediment accumulation rates and lack of fine particles closer to the coast most likely result from resuspension and remobilization of fines from the shelf during winter storms (e.g. Oliveira et al., 2002; Vitorino et al., 2002) (Figure 4.2). The shelf west of Cape Mondego has the coarsest bottom sediments of the investigated shelf area, reflecting stronger bottom dynamics over this region in comparison to the area west of Cape Sines, at comparable distances of the coast. Indeed, the continental margin west of Cape Sines reveals a smoother slope gradient, with the 200 m isobath at only ~20 km off the coast, leading to a more gradual dissipation of tide and wave energy in this region. On the contrary, the much broader and flatter shelf off Cape Mondego changes abruptly into a rather steep slope at 150-200 m water depth, less than 65 km of the coast, resulting in a more abrupt transition between a shallower coarse-grained sediment domain and a deeper fine-grained sediment domain (see Figure 4.1). Lack of sedimentological data from the Estremadura shelf does not allow comparing this region with those above.

Highest percentages of CaCO3 and the lowest molar Corg/Ntot ratios in sediments from the slope of Estremadura spur are in good agreement with previous studies reporting the presence of a coarse and biogenic shelf sediment cover, with calcite content in the silt-clay fraction reaching up to 80 % in the deeper parts of the shelf (Balsinha, 2008). These high carbonate contents suggest bypassing of terrigenous sediment entering via the shelf and through the Cascais and Nazaré canyons, south and north of the spur (Jesus, 2011). Moreover, the low gradient of the shelf and slope at Estremadura spur and great depth of the shelf-break at 330-400 m depth apparently cause a build-up of wave energy as waves approach the coast, sweeping an area of almost 30 km width and preventing fine sediments to deposit (Balsinha et al., 2012). Estremadura spur has also been reported as a hotspot for internal tide generation on the Portuguese margin (Quaresma and Pichon, 2011).

4.5.2. (Paleo)ecology versus taphonomy

In the investigated sediment samples, the smaller coccolith species Emiliania huxleyi and Gephyrocapsa ericsonii displayed concentration values similar or even higher than those of larger coccolith species (≥3 µm), providing a general and qualitative indicator that the assemblages were not significantly affected by dissolution. The occasional presence of intact coccospheres at both shallower and deeper regions (up to 3914 m), even in the context of hydrodynamically active systems as the submarine canyons, is an additional indication of the good preservation of the sediment coccolith assemblages. All the species (both smaller and larger) were more abundant at greater distances off the coast and revealing a negative correlation with sediment particle-size and lithogenic material, mostly reflecting the important bottom water hydrodynamic control on coccolith accumulation in the sediment (data not shown, Guerreiro et al., submitted-c; Chapter 5). Whereas winnowing by waves and currents hampers the accumulation of coccoliths in coarse-grained deposits of the

144 Coccoliths from recent sediments shelf and upper slope, coccoliths will preferentially accumulate in fine-grained hemipelagic deposits that accumulate in more quiescent environments of the middle and lower slope, and the canyons (Figure 4.3). In the upper slope and shelf regions the highest coccolith concentrations were recorded in the southern part of the study area, west of Sines, whereas further offshore, on the open slope, highest coccolith concentrations are recorded further north, west of Mondego. Highest coccolith concentrations in the southernmost sector of the study area, west of Cape Sines, most likely reflect the smoother bottom morphology of this area, leading to a more gradual dissipation of tide and wave energy and favouring the settling of coccoliths and their integration in the sedimentary record. In turn, lower abundances on the upper-slope and shelf off Cape Mondego and Estremadura spur probably reflect strongest bottom hydrodynamics prevailing in these regions, already illustrated by their coarser sedimentary cover (see section 4.5.1). In their earlier study, Abrantes and Moita (1999) also observed higher coccolith abundances along the southern and southwestern Portuguese shelf, and lower abundances on the northern Portuguese shelf, reflecting distinct bottom morphologies, hydrodynamics and depositional conditions prevailing in the two regions. Nevertheless, the presence of more persistently productive conditions off Sines, due to its proximity to the upwelling centre of Cape S. Vicente, should not be discarded. Higher coccolith concentrations of all taxa in the upper canyon reaches, in comparison to adjacent coastal regions (data not shown, Guerreiro et al., submitted-c; Chapter 5), reflect the role of the canyons as preferential depocenters of suspended fine-grained particles, not only terrigenous (e.g. Oliveira et al, 2007; De Stigter et al., 2007), but also biogenic; in this case, both derived from coccolithophore productivity in the overlaying photic layer (vertical flux), and from lateral transport of resuspended coccoliths. Relatively higher abundances in the upper Lisbon-Setúbal Canyon vs. slightly more homogeneous distribution of coccolith abundance values along the Nazaré Canyon axis may be related with differences in the sedimentary settings between the two canyons as discussed in section 4.5.1: trapping of particles derived from vertical flux in the Lisbon-Setúbal Canyon vs. down-canyon transport by tidal currents and sediment gravity flows in the Nazaré Canyon (De Stigter et al., 2007; 2011). Dilution of coccoliths with lithogenic material seems less important than the hydrodynamic control on the coccoliths deposition, in view of the lack of significant negative correlation between coccolith abundance and lithogenic content. Rather, it appears that coccoliths are deposited along with the fine sediment fraction, irrespective of whether that is derived from land or of marine origin. Results strongly suggest that preferential deposition in fine-grained sediments is affecting all the studied taxa equally, and thus coccolith abundances relative to dry sediment weight appears unsuitable for investigating species’ ecological inter- relationships. Species relative abundance (%) within the total of common larger coccoliths will be used hereinafter to infer the species’ ecological inter-relationships independently of bottom sediment dynamics.

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4.5.3. (Paleo)ecological, (paleo)oceanographical and environmental conditions

The observed coccolith species assemblages generally agree with previous studies performed in the Portuguese margin, reflecting the prevailing surface oceanographic circulation and the convergence of water masses from both subtropical and temperate regions (e.g. Cachão, 1993; Guerreiro et al., 2005; 2009). Differences between coastal and oceanic regions, and between the submarine canyons and their adjacent margins reflect the important heterogeneity of the central Portuguese margin, in terms of coccolithophore ecology, oceanographic and sedimentary processes, seabed and coastal topography. Results from factor analysis revealed to be statistically significant (i.e. 70 % of explained variance) and able to summarize the most striking environmental and (paleo)ecological signals preserved in the sedimentary record of the study area (Figure 4.5, Table 4.2). The most distinctive (paleo)ecological assemblages recorded in the sedimentary record are represented in F1 and F3. F1 represents the coast-to-ocean ecological gradient, with C. mediterranea and G. oceanica clearly more abundant closer to the coast, and C. leptoporus further offshore (Figure 4.5a). F3 is represented by two distinct coccolith species assemblages; a coastal assemblage composed by H. carteri, C. mediterranea, G. oceanica particularly important in the Nazaré Canyon, in contrast with G. muellerae which is most common in oceanic waters outside the canyons. G. muellerae is by far the most abundant coccolith species, dominating the assemblages of both coastal and offshore areas in all transects, except on the Estremadura shelf where G. oceanica was more abundant. This broad distribution suggests that this species is optimally adapted for the environmental conditions of the Portuguese margin. The dominance of G. muellerae in sediments from the Portuguese continental shelf has been previously reported by Guerreiro et al. (2005, 2009). Outside the canyons G. muellerae is generally found in highest relative abundance in more open oceanic environments, whereas lower abundances are found closer to the coast (Figures 4.4d and 4.5c). High relative abundances of G. muellerae equal to abundances more typically found in the offshore areas are observed in the upper reaches of the Lisbon-Setúbal Canyon. Since abundances on the adjacent Sines and Estremadura shelves are distinctly lower than in the canyon, the high abundances in this canyon may be interpreted to reflect up-canyon displacement of coccoliths derived from the deeper canyon and slope, along with the overall up-canyon suspended sediment transport that seems to occur in this canyon (De Stigter et al., 2011). Being by far the most abundant species in open slope sediments, any resuspension and up-canyon transport of open slope material will result in an increase of G. muellerae percentages in the upper canyon. This will, at least partially, mask the “real” ecological relationships in this region. On the other hand, given that G. muellerae is the most abundant oceanic species, its increase in the middle Nazaré Canyon and upper Lisbon-Setúbal Canyon in comparison to the adjacent regions, could be tracing the preferential onflow of more oceanic water masses throughout the canyons, as it has been reported to occur in canyon systems (e.g. Skliris and Djenidi, 2006; Guerreiro et al, submitted-a – Chapter 3).

146 Coccoliths from recent sediments

Consistently higher percentages of coccoliths from C. leptoporus further offshore are indicative of its stronger affinity for more oceanic-oligotrophic environments (Figures 4.4a and 4.5a). Previously, Silva et al. (2008) recognized C. leptoporus as a winter-species in Lisbon bay, tracing the advection of subtropical oceanic waters to this region. Guerreiro et al. (submitted-a) (see Chapter 3) observed it thriving further offshore in the Nazaré Canyon, during late-winter. Also with regards to its larger-scale distribution, C. leptoporus is generally more associated to oceanic-oligotrophic environments, preferentially occurring within oceanic gyre centers (Ziveri et al., 2004) and revealing an optimal growth under oligotrophic conditions (Sprengel et al., 2002). That percentages of C. leptoporus are higher on the Sines shelf than on the Estremadura and Mondego shelf may reflect a stronger influence of water masses of subtropical origin in the southern part of the study area. Among the coccoliths showing a preferential near-shore distribution, i.e. G. oceanica, C. mediterranea and H. carteri, high percentages of C. mediterranea in the Nazaré Canyon are particularly interesting because these are in good agreement with a recent study describing the late-winter coccolithophores thriving in this region, where this species was observed to be more abundant in the upper canyon and canyon head (Guerreiro et al., submitted-a; Chapter 3) (Figures 4.4b and 4.5c). The rapid response of C. mediterranea to nutrient availability was recently observed at the shelf-break off Nazaré by Guerreiro et al. (2013) (Chapter 2). Enhanced percentages of C. mediterranea in the canyon head, in comparison to the adjacent coastal areas seems to genuinely reflect its live distribution in this area, possibly reflecting favourable local conditions provided by the canyon near coast. Highest percentages of H. carteri recorded in the northern part of the study area agree to some extent with previous studies performed on the Portuguese margin, reporting an increase of coccoliths from this species in the NW Portuguese shelf (Cachão, 1993; Guerreiro et al., 2005; 2009). An extremely high percentage of H. carteri (~85 %) was found by Guerreiro et al. (2005) in sediments from the mouth of the Douro estuary, interpreted as reflecting an opportunistic behaviour possibly related with locally confined nutrient-rich conditions. Moita et al. (2010) also observed H. carteri to be more abundant in winter west of the Douro River. The important record of H. carteri in the Nazaré Canyon may reflect its ability to thrive in nutrient-rich coastal environments. It may also reflect the good preservation of its large-sized and robust coccoliths in the dynamic bottom environment of the upper Nazaré Canyon. The coastal distribution of coccoliths from G. oceanica in all the five sectors clearly confirms its coastal ecological preference off central Portugal. Our results are in agreement with earlier studies which identified G. oceanica as a typical coastal coccolithophore, well adapted to the nutrient-rich and productive environment found in Portuguese coastal waters (Silva et al., 2008). It is seen as an indicator for maximum upwelling conditions, showing a quick response to nutrient input (Winter et al., 1994; Giraudeau and Bailey, 1995; Broerse et al., 2000; Andruleit and Rogalla, 2002; Sprengel et al., 2002; Andruleit et al., 2003; Guerreiro et al., 2013). The rapid response of this species to favourable nutrient and light conditions was recently observed during a late winter coccolith bloom in the Nazaré Canyon area, where G.

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Chapter 4 oceanica occurred in association with the opportunistic Emiliania huxleyi and small-chain diatoms (i.e. Chaetoceros s.l. and Thalassiosira s.l.) which are indicators of the first stage of upwelling (Guerreiro et al., 2013 – Chapter 2). Highest percentages of G. oceanica observed on the Estremadura shelf are in good agreement with previously reported high coccolith concentrations and relative abundances of this species in surface sediments from the shelf south of the Nazaré Canyon (Guerreiro et al., 2009). Results agree with previous studies which identified the spur as potentially favourable for marine productivity (i.e. Jesus, 2011; Quaresma and Pichon, 2011). Coccolithus pelagicus and the taxonomical group UUR show weaker coast-ocean trends and a weaker signal obtained from factor analysis (Figure 4.4c), possibly reflecting a relatively broader range of ecological preferences in comparison to other coccolithophore species clearly revealing an oceanic (i.e. C. leptoporus) or coastal affinity (G. oceanica, C. mediterranea, H. carteri). For both C. pelagicus and the UUR group there are no noteworthy differences between the submarine canyons and the adjacent shelf and slope. C. pelagicus appears weakly correlated to the coastal-neritic assemblage from F3 reflecting the preferential coastal distribution of this species (Figure 4.5c), which somewhat supports previous studies describing its close relation with the Portuguese upwelling system (Cachão and Moita, 2000; Parente et al., 2004; Narciso et al., 2006; Silva et al., 2008). On the contrary, UUR are notably more abundant at greater distances of the coast, particularly in the southern part of the study area, possibly reflecting the stronger influence of ENACWst water masses in this region (Fiúza et al., 1998). Differences in the coccolith assemblages between the two upper canyons could reflect differences in their environmental settings: (1) a more coastal ecological signature (i.e. C. mediterranea, H. carteri, and somewhat G. oceanica) in the Nazaré Canyon head indicating higher nutrient availability in this area, resulting from the proximity of the canyon head to the coast and the associated intensification of upwelling, and stronger internal tidal activity in the upper canyon. This is supported by Chl-a time series recently obtained from satellite data revealing that the Nazaré Canyon head is the stage of high productivity throughout the year and particularly from March to October, (Guerreiro et al., submitted-a; Chapter 3); and (2) a more oceanic ecological signature in the Lisbon-Setúbal Canyon reflecting more stable and oligotrophic conditions in this area resulting from the more distant position of the canyon heads relative to coastal dynamics. In addition, as mentioned before, influence from ENACWst is also expected to be stronger in the southern part of the study area, and thus, leaving a clearer “oceanic ecological imprint” (i.e. C. leptoporus and UUR) in the Lisbon-Setúbal Canyon. F2 and F4 are mostly reflecting the differences in the sedimentary dynamics between the submarine canyons and the adjacent shelf and slope regions, already discussed in sections 4.4.1 and 4.5.1 (Figures 5b,d).

148 Coccoliths from recent sediments

4.5.4. Coccoliths as (paleo)ecological proxies in coastal regions

Linking living coccolithophore communities to the corresponding coccolith assemblages preserved in seabed sediments is complex, particularly in dynamic coastal areas and in places where the continental margin is dissected by submarine canyons, promoting the interplay of continental and marine factors (e.g. Steinmetz, 1994; Roth, 1994). Sediments in such areas always contain a cumulative averaged signal composed of the sub-signals from all intervening factors, of which only the stronger leave a recognizable “imprint” in the sediment. Our challenge consists in finding the best clues that may lead us to a better understanding of the more important phenomena. Results presented in this study indicate that it is more difficult to make ecological inferences based on coccoliths from the sedimentary record of canyons, in comparison to adjacent margins. The more mixed assemblages of coccoliths in the canyons, including both coastal-neritic and oceanic species, reflects the enhanced exchange of water masses between coastal and oceanic regions through the canyons. However, this exchange may on the one hand involve the advection of living coccolithophores from oceanic to more coastal areas in the upper water masses, whereas on the other hand coccoliths produced by coastal-neritic species in the upper canyon reaches may be transported down-canyon by internal tides and turbidity currents acting along the bottom of the canyon. In the end, we can only interpret the general trends/signals along the canyon by reference to the signal from the surrounding areas (i.e. “background”). Whereas coccoliths appear to be preferentially included in finer-grained sediments, no consistent evidence for selective transport or preservation of individual taxa was found. C. leptoporus and H. carteri, two taxa of comparable sizes and comparable degrees of resistance to dissolution and physical breakage, revealed clearly distinctive distribution patterns unrelated to trends in sediment particle-size. G. oceanica and C. mediterranea, two smaller and more fragile coccolith species, are preferably found closer to the coast despite the stronger winnowing and destructive mechanical forces in that area. Apparent correlations of certain species (e.g. C. leptoporus, H. carteri, G. oceanica and C. mediterranea) with particle-size to our understanding are more likely due to parallel trends in the distribution of these species and particle-size, than representing a causal relationship. Although somewhat diluted, these coast-ocean gradients were also observed in the canyons, even in the Nazaré Canyon, where down-canyon transport of suspended particles continuously occurs, forced by the canyon internal tide. Moreover, the canyons revealed specific features, which are most likely related with the intensified interplay of both sedimentary and ecological factors in these areas (i.e. enhanced percentages of G. muellerae in the Lisbon- Setúbal Canyon head indicating up-canyon transport of resuspended coccoliths and/or preferential onflow of oceanic water masses throughout the canyon; and enhanced percentages of H. carteri and C. mediterranea in the Nazaré Canyon head indicating dissolution and breakage resistance and/or ecological preference for nutrient-rich local conditions in this sector).

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4.6. Conclusions

This study provides new insights into the impact of sea bottom topography and related oceanographic circulation on both taphonomy and ecology of coccolithophores, and the role of submarine canyons as preferential conduits for the onflow of oceanic water masses into more coastal regions, and the down-canyon transport of suspended particles near the bottom. The central Portuguese margin represents a highly heterogeneous region, strongly marked by the presence of two major submarine canyons, the Nazaré and Lisbon-Setúbal canyons, which leave a very distinctive sedimentary and (paleo)ecological signature in seabed sediments from this region. Remarkably high SAR’s and a predominantly lithogenic, organic-rich and fine-grained sedimentary cover clearly distinguishes the canyon’s upper reaches from their adjacent margins. Greater longitudinal homogeneity in sediment composition and texture along the canyons, as compared to the adjacent shelf and slope areas, reflects their function as preferential conduits for the transport of particles towards the oceanic basin. Coccoliths produced by calcareous nannoplankton were found to be useful tracers to investigate (paleo)ecological and (paleo)oceanographic trends prevailing in the central Portuguese margin, supporting previous studies focused on the sedimentary dynamics prevailing in the canyons. The increase of coccolith concentrations further offshore is interpreted as reflecting the oceanic nature of coccolithophores, coupled with physical sorting resulting in preferential accumulation of coccoliths with the finer-grained hemipelagic sediments. Relatively higher coccolith abundances of all taxa in the upper canyons, in comparison to their adjacent coastal regions, reflect the role of the canyons as preferential depocenters of fine-grained sediments, not only terrigenous but also biogenic and including coccoliths derived from local production as well as from lateral transport. Coccoliths from Coronosphaera mediterranea, Helicosphaera carteri and Gephyrocapsa oceanica showed a markedly coastal distribution, revealing to be good (paleo)ecological proxies for enhanced productivity in the upper Nazaré Canyon and Estremadura spur. Calcidiscus leptoporus was consistently better represented further offshore and appeared to be a good proxy for coccolithophore production occurring further offshore. Together with Umbilicosphaera sibogae, Umbellosphera irregularis and Rhabdosphaera spp., this species appears to be tracing the preferential onflow of ENACWst into the southern part of the central Portuguese shelf. Gephyrocapsa muellerae was by far the most abundant species, showing the broadest ecological tolerance, but generally more oceanic, particularly outside the canyons. Enhanced percentages of this species in the upper Lisbon-Setúbal Canyon may be indicating up-canyon transport of resuspended coccoliths from the bottom benthic layer and/or preferential onflow of oceanic water masses through the canyon. The mix of coccoliths from both coastal-neritic and oceanic species in the canyons appears to reflect the enhanced exchange of water masses between more coastal and oceanic regions through the canyons, in comparison to the adjacent shelf and slope regions. Highest percentages of H. carteri and C. mediterranea in the upper Nazaré Canyon, in comparison to

150 Coccoliths from recent sediments the Lisbon-Setúbal Canyon, may be indicative of differences in the environmental conditions between the two canyon systems: greater proximity of the Nazaré Canyon head to the coastline results in a stronger influence of coastal dynamics, characterized by more dynamic and nutrient- rich conditions to which r-selected coccolithophore species are better adapted; on the contrary, higher percentages of coccoliths from G. muellerae, C. leptoporus and UUR in the Lisbon- Setúbal Canyon suggests that a generally more oceanic-pelagic environment prevails in this canyon, explained by its greater distance from the coast and present-day lack of down-canyon sediment transport.

Acknowledgements - Data for this study were collected in the framework of the EU-funded EUROSTRATAFORM (contract EVK3-CT-2002-00079) and HERMES EU-funded projects (contract GOCE-CT-2005-511234), ‘‘Lead in Canyons’’ and “Pacemaker” projects funded by the Netherlands Organization for Scientific Research, and by the Portuguese project Cd Tox-CoN (FCT- PTDC/MAR/102800/2008). Multicores were collected during RV Pelagia cruises funded by the Netherlands Organisation for Scientific Research. Coccolith samples were prepared and analyzed at NANOLAB, CEGUL. A special thanks to all the staff of the Marine Geology Department of the Royal Netherlands Institute for Sea Research (NIOZ), particularly to Wim Boer, Rineke Gieles-Witte, Thomas Richter and Henk de Haas, and to Maria João Balsinha (Portuguese Hydrographic Institute) for collecting the samples from Estremadura shelf. The first author benefited from a PhD grant from the Portuguese Science Foundation (FCT-SFRH/BD/41330/2007).

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Compositional Data Analysis (CoDA) as a tool to study the (paleo)ecology of coccolithophores from the central Portuguese submarine canyons

Chapter 5 Compositional Data Analysis (CoDA) as a tool to study the (paleo)ecology of coccolithophores from the central

Portuguese submarine canyons

Together with M. Cachão, V. Pawlowsky-Glahn, A. Oliveira, A. Rodrigues Submitted to Palaeogeography, Palaeoclimatology, Palaeoecology

Abstract

Submarine canyons are a common feature of most continental margins, and associated with them physical forcing mechanisms exist that may provide a nutrient source for local phytoplankton development. Phytoplankton assemblages characteristic of the canyon setting may be preserved in sediments accumulating within and adjacent to the canyon, but high terrigenous sediment input and strong bottom dynamics are expected to significantly dilute and disturb the (paleo)ecological signal. The main challenge for paleoenvironmental reconstructions consists in extracting the ecological signal from taphonomical distortions, particularly intensified in these contexts. Coccolith assemblages preserved in 89 superficial sediment samples from the Nazaré and Lisbon-Setúbal canyons and adjacent shelf and slope regions off central Portugal were investigated. Results from using classical analytical methods, (i.e. coccolith concentrations - nanno/g; coccolith fluxes - nanno/cm2/yr; and percentages) are compared to results from using Compositional Data Analysis (CoDA) and further discussed. Both coccolith concentrations and fluxes showed spatial trends in which the species’ ecological inter-relationships appear to be masked by taphonomical phenomena, especially towards the coast and in the canyons. Calculation of species percentages relative to the sum of common taxa, eliminating the common sedimentological factors that affect all the taxa equally, revealed distinct ecological signals among the studied taxa. In particular the existence of an assemblage of coastal-neritic affinity, and another of oceanic affinity. Nevertheless, given the spurious correlations and biased statistical analysis associated to percentage determinations, the coastal-neritic and oceanic assemblages and their spatial distribution were validated and confirmed using CoDA, specifically the isometric log-ratio approach (ilr). Providing scale invariance and subcompositional coherence between the components (i.e. taxa), CoDA appears to be a robust statistical tool to study the (paleo)ecology of coccolithophores, corroborating in the present case results derived from percentage determinations. Results clearly confirmed the coastal-neritic distribution of coccoliths from

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Gephyrocapsa oceanica, Helicosphaera carteri and Coronosphaera mediterranea, whereas coccoliths from Calcidiscus leptoporus, Umbilicosphaera sibogae, Umbellosphaera irregularis and Rhabdosphaera spp. more typically occurred offshore. (Paleo)ecological differences between canyons and adjacent shelf and slope areas, and between the two studied canyons, reflect their distinct environmental settings. More pronounced mixing of coccoliths from both assemblages in the canyons reflect the capacity of these structures in promoting the exchange between coastal and oceanic water masses (ecological signal), as well as the role of internal tides and sediment gravity flows in disturbing and homogenizing the sedimentary record (taphonomical signal). Higher “weight” of the coastal-neritic assemblage in the Nazaré Canyon suggests a more dynamic and nutrient-rich environment favourable for coastal opportunistic species to develop, whereas the Lisbon-Setúbal Canyon appears to exhibit more oceanic and stable conditions, probably due to the greater distance of its two canyon heads to the dynamic coastal zone. Results suggest that the (paleo)ecological signal preserved in the studied sediment samples is robust enough to be revealed by the two methods, even within a bottom environment as heterogeneous and dynamic as present on the central Portuguese margin. This study illustrates the potential of percentages in providing a first indication of the most important ecological signals preserved in the sediment and the pointers in which the sequential binary partition will be based on, whereas the ilr is fundamental to test and validate such signals, assuring that all the available information is extracted from the data and that (paleo)ecological interpretations are correctly performed.

Keywords: coccoliths; CoDA; isometric log-ratios; percentages; Nazaré and Lisbon-Setúbal canyons; Portuguese margin

5.1. Introduction

Coccolithophores are the predominant phytoplankton group within calcareous nannoplankton, commonly used as (paleo)environmental proxies and markers of oceanographic processes (e.g. Ziveri et al., 2004; Silva et al., 2008) due to their exceptional fossil record in both open ocean (e.g. Ziveri et al., 2004) and continental shelf/slope sediments (e.g. Cachão and Moita, 2000; Guerreiro et al., 2005; submitted-b; Chapter 4). Although affected by various post- mortem (biostratonomical) mechanisms, studies indicate that coccolith thanatocoenoses preserved in surface sediments can be closely related to the coccolithophore communities dwelling in the overlaying photic layer (e.g. Abrantes and Moita, 1999; Baumann et al., 2000; Kinkel et al., 2000; Sprengel et al., 2002; Boeckel and Bauman, 2008) due to rapid transfer mechanisms mediated by zooplankton grazing (Steinmetz, 1994; Balch, 2004). Thereby, coccoliths provide a particularly useful calibration link with oceanographic conditions since they reflect the physical and ecological patterns that are strong and persistent enough to be preserved in the fossil record (Ziveri et al., 2004). Nevertheless, the correspondence between

156 (CoDA) as a tool to study the (paleo)ecology of coccolithophores

the coccolithophore living communities and the coccolith species assemblages preserved in the seabed is complex, particularly close to the coast and in the context of a continental margin dissected by submarine canyons, where both continental and marine factors interplay. Factors that control the sedimentation of coccolithophores and the distribution of coccoliths in recent (oceanic) sediments have been earlier discussed by Steinmetz (1994) and Roth (1994). Productivity of coccolithophores (P) is primarily a function of light and nutrients, modulated by hydrological parameters like temperature, salinity, turbulence and turbidity (see Margalef, 1978). Seasonal variability in controlling parameters results in successions of seasonally distinct coccolithophore biocoenoses. The coccolith fossil record (FR) preserved in the seafloor sediment results from this primary signal, further affected by several processes here categorized in necrolysis (N), biostratonomy (B), variations in the sediment accumulation rate (SAR), sediment mixing mostly driven from bioturbation (M) and diagenesis (D), all taphonomical phenomena that act upon the coccospheres/coccoliths (Figure 5.1). In other words, whereas a certain P represents the cumulative coccolithophore production of a certain region of the ocean, FR is the cumulative average over several months, years, decades, centuries or even thousands of years of continuous productivity, more or less distorted by taphonomy. For each sampling point, FR can be conceptually represented as follows (equation 1):

∑ ( ) ( ) ( ) ( ) (1) where ti = 1, 2,…, n is time, and PE = (paleo)ecological record, referring to the most recent coccoliths deposited on the seafloorbut prior to burial, i.e. coccolith thanatocoenosis. PE can be considered as the summation of three major components: one here called “weak” ecological signal (PEw), a “strong” ecological signal (PEs) and a third component of biostratonomical nature (PE’) (equation 2):

PE = PEw + PEs + PE’ (2)

PEw represents the ecological component that derives from continuous production of coccolithophores (P1) and results from isolated cell lysis (N1) and/or coccolith dispersion and sinking (B1) through the water column (equation 3).

PEw = P1 × N1 × B1 (3)

Due to their minute dimensions, isolated coccospheres/coccoliths can stay suspended in the water column over extended periods of time, eventually becoming dispersed or even dissolved before reaching the bottom (Roth, 1994; Steinmetz, 1994). For this reason, PEw is considered negligible in terms of contribution to the (paleo)ecological record and thus will not be further considered.

PEs is the stronger ecological signal i.e. able to introduce changes in species inter- relationships in the sedimentary record, controlled by coccolithophore blooms (P2) triggering

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zooplankton grazing (N2), in turn resulting in the incorporation of large amounts of coccospheres in faecal pellets, which are rapidly transported towards the bottom (B2) (equation 4):

PEs = P2 × N2 × B2 (4)

Vertical transport inside faecal pellets is considered the most efficient mechanism for coccoliths to be transferred to the bottom (Steinmetz, 1994). Assuming that zooplankton and nekton are not selective for minute coccolithophore cells, grazing provides a mechanism to efficiently sample coccolithophore assemblages from the upper part of the water column, and packaged in faecal pellets rapidly transferring them to the seafloor, thus contributing to formation of the sedimentary record. Given that biological breakage and dissolution due to grazing probably represent an important alteration factor (Harris, 1994), only the coccolithophores which were incorporated without total destruction into fast sinking faecal pellets or marine snow aggregates are likely to be preserved (Honjo, 1976; 1980). Finally, PE’ represents allochtonous coccolithophore productivity, i.e. advected from adjacent water masses. According to Ziveri et al. (2004), a sediment sample may include coccoliths produced within a geographical area of at least 100 km2, with lateral transport leading to the eventual loss of the smaller and most delicate species. PE’ can also incorporate reworked fossil or subfossil specimens resuspended from the bottom of continental shelf and slope regions. PE’ is particularly important where the continental margin is dissected by submarine canyons, given that these are regions of intensified sedimentary dynamics (i.e. coastal dynamics, internal tides, gravity flows; Arzola et al., 2008; De Stigter et al., 2007; 2011). In equation 2, SAR represents the effect of dilution of the coccolith thanatocoenosis with other sedimentary material (including reworked coccoliths) whereas M represents mixing by organisms living in the benthic sediment layer, both occurring at the seafloor, the latter of which resulting in more or less homogenised coccolith taphocoenoses. After burial, the latter association will be further subjected to diagenesis (D) occurring on longer time scales (i.e. centuries, thousands or millions of years). Processes such as dissolution and recrystallization will tend to preferentially eliminate the smaller and more delicate forms while favouring the preservation of the larger and more robust ones, resulting in an orictocoenosis only partially representing the original assemblage. In conclusion, all these phenomena are represented, for each sampling point, as follows (equation 5):

∑ ( ( ) ( )) ( ) ( ) (5)

PEs is the ecological term that should be extracted from the fossil record, in order to make ecological and subsequent oceanographic inferences. To extract PEs from FR, the effects of advection and reworking (PE’), variations in sedimentation (SAR) and diagenesis (D) must be removed.

158 (CoDA) as a tool to study the (paleo)ecology of coccolithophores

Distortions induced by D can be significantly reduced by: (1) studying Upper Holocene sediment records for which diagenesis can be assumed to be negligible; or (2) selecting species with a similar degree of resistance to dissolution/recrystallization. The (paleo)ecological signal within the thus reconstructed taphocoenosis is now only affected by the biostratonomical advective and reworked components (PE’) and variations on SAR.

Figure 5.1 - Schematic representation of the principal factors that affect the coccolithophore assemblage from the moment of its production (biocoenosis) on the oceanic photic layer towards the moment of its burial (thanatocoenosis -> taphocoenosis-> orictocoenosis). P2 = productivity resulting from coccolithophore blooms, N2 = necrolysis mediated by zooplankton grazing, B2 = rapid vertical transfer of coccospheres within fecal pellets produced by zooplankton, PEs = Strong ecological signal, PE’ = advected and resuspended coccoliths by oceanic currents and bottom resuspension within the bottom nepheloid layer (BNL), SAR = sediment accumulation rate, and D = diagenetic phenomena (e.g. dissolution, recrystallization). The conical shape is meant to schematically represent the area of production (P2) and transport (B2 and PE’) from which a coccolith assemblage preserved in a seafloor sediment sample may be derived.

In the context of a continental margin, the species concentrations (i.e. number of coccoliths per gram of sediment) computed from the taphocoenosis is highly dependent on SAR, which will distort the original thanatocoenosis. Determining the coccolith fluxes (nanno/cm2/yr) from a constant sedimentation rate may eliminate this problem. However, current radiometric methods commonly used for determining sediment accumulation rates in

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continental margin settings provide only averages over decadal to centennial periods of time, lacking desired finer resolution. In addition to that, effects of bioturbation can often not be accounted for in the calculation of sediment accumulation rate, leading to considerable errors especially in slowly-accumulating sediments from open continental slopes (see Carpenter et al., 1982; Fuller et al., 1999; Boer et al., 2006). On the other hand, in regions of high SAR’s such as submarine canyons (De Stigter et al.,

2007; 2011) coccolith fluxes derived from present day productivity (i.e. PEs) end up mixed with resuspended/reworked coccoliths (PE’), due to the fact that these major submarine valleys often act as morphological traps for fine particles in transit along the shelf. Determining species relative abundance in percentage relative to the sum of total or selected common coccoliths is a standard analytical procedure to eliminate the effect of the (common) factors that indiscriminately act upon P, thus allowing to infer species’ ecological inter-relationships independently of sediment dilution effects and/or effects of bottom dynamics. It is thereby assumed that all taphonomical processes affect all coccolithophore species of similar size (≥ 3µm) equally. This way, only the original PEs and PE’ signals will remain. Nevertheless, the closure problem and the inconsistency of determining percentages may lead to spurious correlations and biased statistical analysis; according to Pawlowsky-Glahn and Egozcue (2006), using percentage values leads to inconsistent and spurious relations between the parts and, thus, to potentially unrealistic interpretations (i.e. changing the number of components leads to different relationships among them). There are cases where it is possible to obtain similar results, especially when the sub-compositions are nearly constant/homogeneous, although one cannot assure that it will be so in advance. Compositional Data Analysis (CoDA) (Buccianti and Esposito, 2004; Pawlowsky-Glahn and Egozcue, 2006) was designed to provide robust results, since the inferences made on the coccoliths assemblage is based on a theoretical approach that provides tools that allow to extract relative information while satisfying scale invariance, subcompositional coherence and permutation invariance. By implementing the use of isometric log-ratios, CoDA makes the treatment of two variables, or groups of variables, symmetric, given that Log (x/y) = - Log (y/x). Such symmetry is essential to avoid spurious correlations by giving them subcompositional coherence, and thus leading to more reliable comparisons and interpretations. Here, CoDA is applied to study the (paleo)ecology of coccolithophores from the central Portuguese margin. The isometric log-ratio (ilr) approach was applied to previously reported coccolith assemblage data from superficial sediments collected along the Nazaré and Lisbon- Setúbal canyons and adjacent shelf and slope regions (Guerreiro et al., submitted-b; Chapter 4), to validate the robustness of ecological inferences based on percentages. The goals of the present work are: (1) to confirm the effect of submarine canyons on the (paleo)ecology of coccolithophores, (2) to extract the ecological signal, independent from the intensified taphonomical effects in these regions (i.e. PE’ and SAR), and (3) to introduce the isometric log- ratio as a procedure to validate and obtain consistent (paleo)ecological interpretations. Results obtained from both compositional (CODA) and classical approaches are compared and discussed.

160 (CoDA) as a tool to study the (paleo)ecology of coccolithophores

5.2. General principles behind Compositional Data Analysis

Compositional data are data in which the components represent “parts of a whole”. They carry only relative information between parts, and are usually represented as percentages or ppm; in this case, their sum corresponds to a constant, typically 100% or 106 (Parent et al., 2012). Because of this, compositional data are an easy target of spurious correlations and subcompositional incoherence that typically affect all data that measures parts of the same whole. An example: considering an ecological subsystem composed of a few selected species (sp1, sp2, sp3,…) the behaviour of any two components will randomly change their signs and meanings depending on the other components involved, leading to the so-called “spurious correlation problem” or subcompositional incoherence (Pearson, 1897; Tolosana-Delgado, 2012; Buccianti, 2013). Ideally, results should not depend on whether we take one, some, or all of our components or species, neither on whether we scale them up and down by arbitrary numbers, nor even whether we choose our samples to sum up to 100% or leave them untouched (Aitchison, 1997). To avoid these problems, a “scale or scaling invariance” property should be inherent to the methods applied when studying compositional data. Such property is assured by using the ratios between the components instead of their individual variation, based on the premise that one cannot assess absolute increase or decrease of the components, but only relative changes (Aitchison et al., 2000). Despite these facts, most of the quantitative analyses performed by geoscientists all over the world do not take into account the particular features of compositional data. Although similar results may be achieved from both classical and compositional approaches, depending on where the data are located within the sample space or simplex (i.e. if they are close to the centre or to the borders), it is up to now not possible to know the weight of this effect a priori, or how to measure it. Therefore, part of the information about compositional natural systems may become completely lost or misunderstood (Buccianti, 2013). Compositional Data Analysis (CoDA) is a set of statistical tools and geometric concepts built with the purpose of allowing results to satisfy scale invariance and subcompositional coherence, based on the idea that we can only assess relative changes between components (Aitchison, 1997). It requires transformation of compositional data located in the constrained space (the simplex) before performing statistical analysis, in order to move them into real space, thus allowing the inference about the sample features, from which the data are drawn, to be consistently performed from a theoretical point of view (Aitchison, 1982; Buccianti and Esposito, 2004). By avoiding spurious correlations and negative bias, the log-ratio approach permits obtaining an exhaustive understanding on how natural phenomena work, and to extract all the information contained in data variability (Buccianti, 2013). Given the Euclidean space nature of the simplex (Pawlowsky-Glahn and Egozcue, 2001), representing compositions by their coordinates in the simplex has an enormous potential. A suitable orthonormal basis for this purpose is obtained through an isometric log-ratio transformation (Egozcue et al., 2003). The advantage of such a transformation is that, as a result

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of orthogonality, the original information is preserved (Parent et al., 2012), i.e. the distance between two observations before and after the transformation is the same. To obtain an interpretable isometric transformation and provide the geometry required to analyse data in Euclidean space, Egozcue et al. (2003) and Egozcue and Pawlowsky-Glahn (2005a) arranged the D parts of a composition in a D-1 sequential binary partition (SBP), which leads to an orthonormal basis. A SBP is a hierarchical grouping of parts of the original compositional vector, starting with the whole composition as a group and ending with each part in a single group (Egozcue and Pawlowsky-Glahn, 2005a). This partition can be selected by the user in order to enable the best interpretation of the results when some kind of relation between parts is a priori known or preferred (Thió-Henestrosa et al., 2008). The D-1 isometric log-ratio (ilr) coordinates are data transformations mapped according to the SBP and computed as contrasts/balances between two groups (tagged with + and – signals) (Parent et al., 2012). Such balances reflect the relative variation of two groups of parts, i.e. the isometric log-ratios of geometric means of groups of parts (see Egozcue and Pawlowsky-Glahn, 2005a). The balance-dendrogram is a new methodology within CoDA aimed to explore and describe compositional data in a coherent geometry, particularly useful to summarize and to graphically describe a composition of many parts. It allows the visualization of the partition used and, for each balance, the sample mean or centre, the proportion of the sample total variance corresponding to it, and summary statistics represented by the boxplot of percentiles 5, 25, 50, 75 and 95 (see Thió-Henestrosa et al., 2008). A more complete description of the elements of the balance-dendrogram is presented by Egozcue and Pawlowsky-Glahn (2005b) and Thió-Henestrosa et al. (2008).

5.3. Regional setting

The central Portuguese margin has a relatively narrow shelf (20–50 km wide and a gradient of <1°), passing into a steep irregular slope (6–7°) below the shelf-break which is located at 160-200 m depth. The shelf is composed of thick Cenozoic carbonate and detritic formations, filling structural basins formed during earlier rifting phases. The margin is dissected by a number of long submarine canyons, of which the Nazaré and Setúbal–Lisbon canyons are the most remarkable (e.g. Vanney and Mougenot, 1981; Mougenot, 1989; Alves et al., 2003) (Figure 5.2). The Nazaré Canyon stands out for being one of the largest and steepest canyons of the European margin, cutting across the full width of the Portuguese central margin almost to the coastline. The canyon starts at ~50 m water depth and within 1 km from Nazaré Bay, and extends to the Iberian Abyssal plain, 211 km off the canyon head. This canyon is presently not connected to a major modern drainage system, and obtains its sediment input by capture of particles transported by littoral drift (Duarte et al., 2000) and along the shelf (Oliveira et al., 2007; De Stigter et al., 2007). Tidal currents actively resuspend and transport sediment in the upper-middle canyon, as reflected by high concentrations of suspended particles in bottom

162 (CoDA) as a tool to study the (paleo)ecology of coccolithophores

waters, high horizontal and vertical sediment fluxes in the bottom water layer, and high sediment accumulation rates on the seabed (De Stigter et al., 2007). Sediment accumulated in the canyon head and upper section is remobilized and flushed to its lower section and adjacent abyssal plain by intermittent sediment gravity flows occurring mostly during autumn and winter months (De Stigter et al., 2007; Martín et al., 2011; Masson et al., 2011). The Lisbon-Setúbal Canyon has a more complex morphology, fed by two main branches: the E-W oriented Setúbal branch and the N-S trending Lisbon branch. Like the Nazaré Canyon, the latter is deeply incised into the continental shelf and slope, and extends down to the abyssal plain at depths > 4800 m. Different from the Nazaré Canyon, however, the Lisbon-Setúbal Canyon heads, located in somewhat deeper water a few km off the coast, are connected with two major river systems, i.e. Tagus and Sado rivers (at 120 and 90 m depth, and at 20 and 13 km off the river mouths, for the Lisbon and Setúbal branches, respectively (see Lastras et al., 2009). Recent findings of De Stigter et al. (2011) indicate that the Lisbon Setúbal-Canyon is presently nearly inactive in terms of down-canyon sediment transport, probably due to the presence of an overall up-canyon direction of net water transport, leading the particles to settle in the upper canyon towards the canyon head rather than disperse them down-canyon, and the apparent rareness of sediment gravity flows, which in other canyon systems (e.g. Nazaré Canyon) are the dominant mechanism of down-canyon dispersal. Fine-grained predominantly lithogenic particles from the adjacent shelf areas accumulate in their upper reaches, whereas the sediment deposited further down in the middle and lower canyon reaches is essentially hemipelagic, similar to the sediment found on the adjacent continental slope. Circulation over the Portuguese shelf and upper slope displays a marked seasonal variation associated with seasonal shifts in the position of the Azores high and Iceland low pressure systems (e.g. Haynes et al., 1993; Barton, 2001; Relvas et al., 2007). During summer, the Azores high migrates towards the central Atlantic, typically inducing Trade Winds to become northerly, inducing an equatorward circulation over the upper 150-200 m of the water column off Portugal. Under such conditions, the surface layer of about 30 m thick of relatively warmer and lighter water is swept offshore by Ekman transport, allowing colder, less salty and nutrient enriched subsurface water to rise to the surface along the coast (e.g. Fiúza, 1983; Haynes et al. 1993; Barton, 2001; Relvas et al., 2007; Alvarez et al., 2011). During winter, the Iceland low intensifies and the dominant wind regime becomes southerly along the western Portuguese margin. This induces the IPC to rise over the upper slope and shelf, where the poleward flow produces an onshore Ekman transport, in turn resulting in downwelling conditions over the shelf (Fiúza, 1983; Vitorino et al., 2002). The upper 500 m of water column off Portugal, including the surface mixed layer and the first thermocline, is constituted by the Eastern North Atlantic Central Water (ENACW). This water mass, representing the main source of nutrient-rich waters upwelling along the Portuguese coast, shows considerable variation in its hydrological features as it travels along the coast (Fiúza, 1984; McCave and Hall, 2002). The ENACW has two main components of different origin, converging to this region: a lighter, relatively warm and salty subtropical branch (ENACWst) formed along the Azores Front, which gradually loses its characteristics as it

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travels further northwards along the Iberian margin; a less saline colder water mass of subpolar origin (ENACWsp) slowly flowing southwards below the poleward subtropical branch, related with the Subpolar Mode Water formed in the eastern North Atlantic by winter cooling and deep convection (Fiúza et al., 1998).

Figure 5.2 - Geographical location of the central Portuguese margin. Black squares represent locations where multi- and boxcore sampling was performed for the study of coccoliths. Grey squares represent locations where coccolith fluxes were determined from sediment accumulation rates (SAR).

164 (CoDA) as a tool to study the (paleo)ecology of coccolithophores

5.4. Material and Methodology

5.4.1. Cruises and surface sediment sampling

The sediment samples used in this study were recovered during several cruises with RV Pelagia of Royal NIOZ, held in November 2002, October 2003, April/May 2004, May 2005, September 2006 and March 2011 in the central Portuguese margin (cruises 64PE204, 64PE218, 64PE225, 64PE236, 64PE252 and 64PE332, respectively). Surface samples were collected with equipment and methodology as described in De Stigter et al. (2007, 2011). Samples corresponding to the top 0.5 or 1 cm of box- and multicores were sub-sampled and analysed to determine the recent coccolith assemblages. Sediment coring was concentrated on six transects crossing the central Portuguese margin in an approximately E- W direction, aiming to represent the gradients coast versus ocean and canyons versus adjacent shelf and slope: (1) three transects along the axis of the Nazaré, Lisbon-Setúbal and Cascais canyons; (2) three transects covering the shelf and open continental slope off Cape Mondego, Estremadura spur and off Cape Sines. Coring positions are shown in Figure 5.2 and listed in Appendix D.

5.4.2. Laboratory and microscope analysis

For the study of the fossil record of coccolithophores, 89 surface sediment samples were analysed. Slides were prepared following the random settling procedure (Flores and Sierro, 1997) and observed under optical polarizing microscope (Olympus BX-40), at 1250× magnification. A minimum of 300 individual coccoliths (i.e. “nanno” for short) was counted and identified in each slide to determine their concentration (nanno/g), according to the following equation:

V Pa 1 N  n    (6) Vp Oa W where, N = nanno/g, n = number of counted coccoliths, V = volume within the glass bottle (10000 µl), Vp = volume pipetted and injected into the Petri dish, Pa = Petri dish area, Oa = observed area (obtained by the number of vision fields, VF, at the microscope, multiplied by the unit area corresponding to the microscope; 1 VF Olympus BX-40 = 0.02 mm2), and W = weight of the sediment sample. The numbers of coccoliths per gram of sediment will be generally referred to as “coccolith concentrations” throughout the text, to distinguish them from the “relative abundances” calculated relative to the sum of common coccoliths. At each sampling point, coccolith fluxes (nanno/cm2/yr) were determined by multiplying the coccolith concentrations by sediment accumulation rates (SAR), previously calculated from sediment profiles of 210Pb (22.2 years half-life (De Stigter et al., 2007; 2011; Guerreiro et al., submitted-b, Chapter 4).

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To minimize effects of differential dissolution, only the larger and more robust taxa (≥ 3 µm) were considered. Nine coccolithophore taxa were selected for this study: Calcidiscus leptoporus (Cl), Coronosphaera mediterranea (Cm), Coccolithus pelagicus s.l. (Cp), Gephyrocapsa muellerae (Gm), Gephyrocapsa oceanica (Go), Helicosphaera carteri (Hc), Umbilicosphaera sibogae, Umbellosphaera irregularis and Rhabdosphaera spp. Due to their scarcity and the fact that all the three latter taxa are considered as tracers for the onflow of oceanic warmer currents driven along the Azores current onto the Portuguese shelf (Cachão et al., 2000) they were grouped into one single taxonomic variable (UUR). Relative abundances (%) were determined relative to the sum of the seven taxonomic groups (≥ 3 µm).

5.4.3. Statistical analysis: compositional and classical approaches

The isometric log-ratios (ilr) (Egozcue et al., 2003) were determined from the coccolith concentrations (nanno/g) and made by taking rigorously into account the sample space of compositional data (i.e. data matrices whose rows sum to 100%). Six compositional balances (β) were determined by applying a sequential binary partition (SBP) to the seven taxonomic groups, based on our pre-acquired knowledge of their ecological preferences and on the results from percentages (e.g. Winter et al., 1994; Cachão and Moita, 2000; Cachão et al., 2000; Silva et al., 2008; Guerreiro et al., submitted-b, Chapter 4), determined according to: Σ 7 taxa (%) = Cl (%) + Cm (%) + Cp (%) + Gm (%) + Go (%) + Hc (%) + UUR (%) = 100 %. The SBP was performed by taking the whole group (7 taxa) and dividing it into two groups (here 4 neritic- coastal taxa vs. 3 oceanic taxa). The resulting balance (β1) reflects the (geometric) mean behaviour of the first group vs. the (geometric) mean behaviour of the second group. Each group was subsequently divided again until each group was represented by one single species (see Table 5.1).

43 4 CpGo  Hc Cm β1 { Cp, Go, Hc, Cm} vs { Gm, Cl, UUR } =  LN (7) 4  3 3 Gm ClUUR

2 2 2 CpGo β2 {Cp, Go} vs {Hc,Cm} =  LN (8) 2  2 2 Hc Cm

11 1 Cp β3 {Cp} vs {Go} =  LN (9) 1  1 1 Go

11 1 Hc β4 {Hc} vs {Cm} =  LN (10) 11 1 Cm

21 2 Cl UUR β5 {Cl, UUR} vs {Gm} =  LN (11) 2 1 1 Gm

11 1 Cl β6 {Cl} vs {UUR} =  LN (12) 11 1 UUR

166 (CoDA) as a tool to study the (paleo)ecology of coccolithophores

The balance-dendrogram representing the six isometric log-ratios was automatically obtained using CoDAPACK software (Version 2.01.13) and calculated according to the following equations, where ln stands for the natural logarithm, or logarithm to the base e: A priori it is assumed that the largest compositional changes occur along a coast to ocean gradient, and thus, the coccolith concentrations, fluxes and percentages of each taxonomic group, and the ilr’s of each compositional balance, were plotted against distance to the coastline (expressed in km) and compared. Boxplots representing the distribution of the isometric log- ratios (ilr) in water depth (m) were also built for the five studied sectors.

5.5. Results

5.5.1. Classical approaches: nanno/g, coccolith fluxes and percentages

Data of coccolith total counts, concentrations (nanno/g), fluxes (nanno/cm2/yr) and relative abundances (%) determined from the studied sediment samples are listed in the Appendix D. With the exception of the coccolith fluxes, results presented in this section have been previously discussed in Guerreiro et al. (submitted-b) (see Chapter 4) and, therefore, only a general overview of the coast to ocean distribution of coccolith species is shown. A general decrease of coccolith concentrations (nanno/g) towards the coastline is visible from the plots of the seven taxonomic groups, especially in the case of Cl. Such W–E decreasing gradient is particularly evident along the ocean-coast transects adjacent to the submarine canyons, whereas all taxa display higher nanno/g values in the upper sections of the canyons in comparison to the adjacent coastal regions, particularly in the upper Lisbon-Setúbal Canyon (Figure 5.3). Coccolith fluxes (nanno/cm2/yr) determined from SAR’s were highest at the central part of the investigated region, with a maximum value in the Nazaré Canyon head, where several coccolith species recorded a peak in flux. Indeed, a clear distinction between the submarine canyons and the adjacent coastal regions is noticed close to coast: higher coccolith fluxes are recorded in the upper reaches of the canyons, particularly in the Nazaré Canyon, whereas rather low fluxes are noticed in the adjacent regions, for comparable distances to the coast. Cp, Gm, Go and Hc recorded their highest coccolith fluxes in the upper reaches of the canyons, particularly in the Nazaré Canyon (Figures 5.3c-f). Cl and UUR recorded similar values of coccolith fluxes in both studied canyons (Figure 5.3a, g). Further offshore, generally low coccolith fluxes were obtained, except on the open slope of Estremadura spur. Most of the species recorded an increase of coccolith flux in this region, but it was most pronounced for the oceanic taxa Cl, Gm and UUR (Figures 5.3a, d, g). Species relative abundances also show a clear W-E gradient, in this case revealing differences among the taxa. An increase in percentage of the neritic-coastal species Cm, Go and Hc towards the coast is clearly recorded, with Cm and Hc clearly more abundant in Nazaré

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Figure 5.3 – Coccolith concentrations (nanno/g), fluxes (nanno/cm2/yr) and percentages plotted against distance to coast (km): (a) Calcidiscus leptoporus, (b) Coronosphaera mediterranea, (c) Coccolithus pelagicus.

Figure 5.3 (cont) – Coccolith concentrations (nanno/g), fluxes (nanno/cm2/yr) and percentages plotted against distance to coast (km): (d) Gephyrocapsa muellerae, (e) Gephyrocapsa oceanica.

Figure 5.3 (cont) – Coccolith concentrations (nanno/g), fluxes (nanno/cm2/yr) and percentages plotted against distance to coast (km): (f) Helicosphaera carteri, (g) Umbillicosphaera sibogae, Umbellosphaera irregularis, Rhabdosphaera spp. (UUR)

(CoDA) as a tool to study the (paleo)ecology of coccolithophores

whereas Go is more abundant on the Estremadura shelf. Cp also reveals this general trend although weaker than the previously mentioned species. Cl displays the opposite spatial distribution, clearly increasing further offshore. Relatively higher percentages of this species are noticed at Lisbon-Setúbal Canyon. Gm and UUR display the same general decreasing trend towards the coast, although less distinctive than in Cl. Gm has markedly higher relative abundances in the upper reaches of the canyons in comparison to the adjacent shelf and coast, particularly in the Lisbon-Setúbal Canyon. Higher proportions of coccoliths from oceanic taxa are noticed at the upper Lisbon-Setúbal Canyon, whereas the coccoliths from coastal-neritic species are better represented at the upper Nazaré Canyon (Figure 5.3).

5.5.2. CoDA: isometric log-ratios (ilr)

The dendrogram represented in Figure 5.4 gives information about the relative importance of each (paleo)ecological assemblage (oceanic vs. coastal-neritic) within the investigated sectors. Each balance (β) is represented by a black vertical "arm", the length of which is proportional to the variance explained by the balance, if all the samples are considered together, i.e. as one unique sample. The relative weight of each (paleo)ecological signature in the different sub-groups of samples (i.e. investigated sectors) is given by the horizontal distance between the box plot and the black vertical "arm" corresponding to the centre of the balance, i.e. the shorter it is towards the centre of the balance, the heavier is its geometric mean in the data set. It means that the geometric mean weighs more in that specific group of samples. Each sector (assumed to be well represented by a group of samples) is illustrated by a box plot and a "vertical arm" with the same colour, the length of both giving information about the compositional variability (i.e. > length = > variability). The position of the vertical "arm" in the box plot indicates the mean of the balance in that specific sector. The performed SBP, the mean and variance of each extracted isometric log-ratio (i.e. balance) is represented in Table 5.1. The ilr’s obtained for each sediment sample are listed in the Appendix D. The most striking differences between the five sectors shown in the dendrogram are given by β1, which discriminates the coastal-neritic from the oceanic taxa, i.e. β1 represents the (geometric) mean behaviour of the neritic-coastal group (Cm, Hc, Go and Cp) vs. the (geometric) mean behaviour of the oceanic group (Gm, UUR and Cl). This first balance indicates that the oceanic taxa have a higher weight on the studied dataset, as revealed by the relatively shorter “horizontal left arm” compared to the corresponding horizontal right arm, i.e. the vertical arms are globally positioned closer to the oceanic group. When comparing the five sectors, the graph clearly shows the relatively stronger relation of the canyons with the coastal-neritic species, as indicated by the median of their boxplots which is relatively displaced towards the right side of the dendrogram, particularly in the case of Nazaré Canyon. On the contrary, for the shelf and slope regions the median coccolith abundance is displaced toward the left side of the dendrogram, meaning that in these sectors the oceanic assemblage has a higher weight. The region west of Cape Sines appears as the most strongly

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Figure 5.4 - Balance-dendrogram representing the six balances resulting from the SBP previously applied to the original composition of seven taxonomic groups. Samples were previously organized according to the sector where they were collected. Each boxplot refers to a specific sector: black = off Cape Mondego, orange = Nazaré Canyon, light blue = Estremadura spur, green = Lisbon-Setúbal Canyon, dark blue = off Cape Sines. The taxonomic group UUR is graphically represented by Umbilicosphaera sibogae, due to its higher abundance.

(CoDA) as a tool to study the (paleo)ecology of coccolithophores

Table 5.1 – Results from the SBP applied to the original composition of seven taxonomic groups, mean and variance of the six extracted isometric-ratios (i.e. balances = β).

ILR binary partition: Balance Cp Hc Cl Go Gm Cm UUR Mean Variance β1 1 1 -1 1 -1 1 -1 -0.8 1.5 β2 1 -1 0 1 0 -1 0 0.3 0.2 β3 1 0 0 -1 0 0 0 -1.4 0.2 β4 0 1 0 0 0 -1 0 -0.3 0.3 β5 0 0 1 0 -1 0 1 -2.3 0.4 β6 0 0 1 0 0 0 -1 0.5 0.4

related with the oceanic coccolith assemblage, whereas the shelf and slope regions west of Cape Mondego and Estremadura spur reveal stronger mixing of coccoliths from both oceanic and coastal-neritic taxa. When comparing among coastal-neritic species (β2, β3 and β4) and among oceanic taxa (β5 and β6), no significant differences between the investigated sectors are noticed. The Nazaré Canyon and the region west of Cape Sines reveal a slightly higher “weight” of coccoliths from Cm and Hc, whereas the regions west of Cape Mondego, Estremadura spur and the Lisbon- Setúbal Canyon reveal a slightly higher “weight” of coccoliths from Go and Cp. β5 shows the greater importance of Gm in comparison to UUR and Cl, as indicated by the shorter “arm” that separates Gm from the centre of β5. Gm is more important in the Mondego transect and in the canyons in comparison to the Estremadura and Sines transects. In order to complement the information given by the balance-dendrogram and to achieve a clearer perception about the spatial distribution of the (paleo)ecological ratios along the five studied sections, the ilr’s obtained from the SBP were plotted against distance to coast (Figure 5.5). In analogy to factor scores in classical factor analysis (see Guerreiro et al., submitted-b; Chapter 4), the distribution of ilr’s towards the positive and negative part of the yy axis indicates the relative importance of the species in the numerator and denominator of each isometric log-ratio (i.e. balance), respectively, within the studied samples (cases). The balance β1 clearly reveals a relatively higher importance of oceanic species further offshore (negative values), whereas the coastal species become more important closer to the coast (positive values). A larger number of samples recording ilr values < 0 reflects the higher “weight” of the oceanic assemblage within the study area, most probably due to the remarkable dominance and broad distribution of Gm. Balance β1 is more stable further offshore than closer to the coast (< 80 km), i.e. a very stable proportion between coastal and oceanic taxa is noticed within and among the studied sectors offshore (except in the Lisbon-Setúbal Canyon, due to lack of data for this offshore region), whereas a higher variability is visible towards the coast. The positive trend of β1 towards the coast is more distinct outside the canyons, whereas a higher variability of both assemblages is noticed in the upper reaches of the canyons (Figure 5.5a). At comparable (proximal) distances off the coast, a larger number of samples with negative ilr’s in the Lisbon-Setúbal Canyon suggests a higher “weight” of the oceanic group in

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Chapter 5 this canyon, whereas the larger number of samples with positive ilr’s in the Nazaré Canyon indicates a higher “weight” of the coastal-neritic. When comparing the shelf and slope regions adjacent to the canyons, samples collected off Cape Sines stand out for having ilr’s ≤ 0 along the entire W-E transect, suggesting a more oceanic environment in comparison to the regions off Cape Mondego and Estremadura spur where a higher “weight” of the coastal-neritic assemblage is noticed near the coast. The remaining balances (ilr’s) reveal a more uniform lateral distribution in comparison to β1, although here too a higher stability further offshore is observed, in comparison to increasing variability towards the coast. The distribution of ilr’s indicates that among the coastal-neritic group, Go represents the higher weight within the dataset, followed by Cm, Hc and Cp. (Figures 5.5b-d). Outside the canyons, β2 tends to increase towards the coast revealing a higher “weight” of Cp and Go in these proximal regions. In contrast, the Nazaré Canyon reveals a generally decreasing trend along its entire W-E section, with the strongest signal of Hc and Cm recorded close to the coast (~20 km). At the Lisbon-Setúbal Canyon, β2 stands out for recording a rather uniform lateral distribution (Figure 5.5b). Among the oceanic taxa, Gm displays by far the highest weight in the studied samples, followed by Cl and UUR. Balance β5 reveals a strikingly uniform W-E distribution trend in the shelf and slope regions west of Cape Sines and Estremadura spur, whereas the submarine canyons and the region off Cape Mondego reveal a clearly decreasing trend from 60-40 km to the coast (Figure 5.5e). Balance β6 reveals a quite uniform lateral distribution, although a certain decreasing tendency is noticed towards the coast, suggesting that Cl is more important further offshore in comparison to UUR (Figure 5.5f). In Figure 5.6, the box-plots representing the distribution of the six balances with water depth (deeper or shallower than 500 m) revealed similar spatial distributions to those from Figure 5.5. The most striking aspects refer to the distribution of β1 and β5, whereas the remaining balances revealed a quite uniform distribution among the five sectors, at both shallow and deeper water regions (Figures 5.6a and 5.6e). Higher variability is often noticed for water depths lower than 500 m, whereas the deeper regions reveal a more uniform N-S distribution. β1 reveals a conspicuous mix of both coastal and oceanic taxa at both shallower and deeper areas along the canyons, whereas a clear separation between coastal and oceanic taxa is noticed on the adjacent shelf and slope regions, at shallower and deeper areas, respectively. The Nazaré Canyon shows the stronger mixing between the two assemblages and the highest weight of coastal coccoliths at both water depth ranges (particularly at < 500 m), whereas the Lisbon- Setúbal Canyon has a higher weight of oceanic taxa at both water depth ranges. The coastal coccolith assemblage reveals a general N-S decrease of weight at < 500 m, whereas the canyons have a higher weight of the coastal assemblage at > 500 m, in comparison to the adjacent shelf and slope regions (Figure 5.6a). β5 illustrates a general N-S decreasing importance of Gm in the shallower areas, except in the upper reaches of the canyons where it was more strongly recorded in comparison to the adjacent shelf and slope regions at comparable water depths. Towards greater depths, an increase in importance of Cl and UUR is noticed in all the sectors. β6 shows almost no

174 (CoDA) as a tool to study the (paleo)ecology of coccolithophores variability within and among the five studied sectors, with the exception of the Sines transect (Figure 5.6f).

Figure 5.5 – Isometric log-ratios (ilr) obtained for the studied set of samples plotted against distance to coast (km): (a) β1 [Cp, Go, Hc, Cm / Cl, UUR, Gm], (b) β2 [Cp, Go / Hc, Cm], (c) β3 [Cp / Go], (d) β4 [Hc / Cm], (e) β5 [Cl, UUR / Gm], (f) β6 [Cl / UUR].

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Figure 5.6 – Boxplots representing the distribution of the isometric log-ratios (ilr) in water depth (m), along the five studied sectors: (a) β1 [Cp, Go, Hc, Cm / Cl, UUR, Gm], (b) β2 [Cp, Go / Hc, Cm], (c) β3 [Cp / Go], (d) β4 [Hc / Cm], (e) β5 [Cl, UUR / Gm], (f) β6 [Cl / UUR].

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5.6. Discussion

5.6.1. (Paleo)ecology of coccolithophores based on isometric log-ratios

Results presented in this study are in good agreement with distribution trends previously reported by Guerreiro et al. (submitted-b) (see Chapter 4) for this dataset, using factor analysis with the taxa percentages: distinct (paleo)ecological N-S and W-E trends were observed between the seven taxonomic groups, and differences were also observed between the submarine canyons and the adjacent shelf and slope regions. The relatively higher “weight” of the oceanic assemblage in the studied dataset reflects the significant dominance and broad distribution of Gm (Figure 5.4). Of the three oceanic species, Gm seems to be better adapted to more turbulent and nutrient-rich coastal regions. Although this species has been associated to more temperate ecological conditions (Ziveri et al., 2004) and to colder water masses at the onset of upwelling west off Portugal (Silva et al., 2008), its high abundance and wide distribution in the sedimentary record suggests it has a broad ecological tolerance in the central Portuguese margin. The relative enrichment of coccoliths from Gm in the upper reaches of the Lisbon-Setúbal Canyon may result from up-canyon transport of resuspended coccoliths within the benthic boundary layer toward the canyon head (De Stigter et al., 2011) and/or the preferential onflow of more oceanic water masses through the canyons, as has been reported to occur in canyon systems (e.g. Skliris and Djenidi, 2006; Guerreiro et al, submitted-a; Chapter 3) (Figure 5.4 and 5.5e). On the contrary, Cl and UUR were more persistently associated to more oceanic regions and therefore may be used as proxies for coccolithophore productivity (P) occurring offshore (Figures 5.5a and f). The relatively higher weight of Cl and UUR at the southernmost part of the study area (i.e. west of Cape Sines) and the N–S decreasing importance of the coastal-neritic assemblage in the shallower areas possibly reflects a stronger influence from ENACW of subtropical origin (ENACWst) in this region (Fiúza et al., 1998; Guerreiro et al., submitted-b; Chapter 4). Such subtropical influence will expectedly be stronger during winter when the Iberian Poleward Current advects NEACWst towards the Portuguese coast under downwelling conditions prevailing during this season (Vitorino et al., 2002). Whereas the coastal-neritic taxa were preferentially distributed closer to the coast in all the five sectors, distinct (paleo)ecological signatures were observed in the canyons and the adjacent shelf and slope regions at greater water depths, most probably reflecting differences in terms of oceanographic and bottom sedimentary dynamics. In the canyons, particularly at Nazaré Canyon, higher “weight” of coccoliths from coastal-neritic species, higher mixing between the two assemblages (dispersion) (Figures 5.4, 5.5a, 5.6a) may reflect the capacity of the canyons to create nutrient-rich conditions favouring growth of opportunistic species, and to promote the exchange of water masses from neritic-coastal and oceanic regions (i.e. ecological signal). It may also reflect the effect of permanent internal tidal activity resuspending and remobilizing fine sediments from the canyon seafloor, producing a relatively more

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Chapter 5 homogeneous sedimentary cover (taphonomical signal, PE’) (De Stigter et al., 2007; 2011; Guerreiro et al., submitted-b; Chapter 4). Of the five sectors, the Nazaré Canyon reveals the highest dispersion and the highest weight of coastal-neritic coccoliths at >500 m depth, in comparison to the other sectors for the same depth range, including the Lisbon-Setúbal Canyon (Figure 5.6a). On the one hand, given the proximity of the Nazaré Canyon head to the coastline, this major valley is likely able to advect living coccolithophores from oceanic to more coastal areas and, at the same time, influencing oceanographic circulation near the coast (i.e. upwelling intensification, internal tidal activity), favouring the input of nutrients and thus promoting the development of r-selected species. Chl-a data recently obtained from satellite imagery (2006-2011) suggest that the Nazaré Canyon head is the most persistently productive part of the upper-middle canyon (Guerreiro et al., submitted-a; Chapter 3), supporting this hypothesis. On the other hand, internal tidal activity and intermittent down-canyon sediment gravity flows in this canyon were observed redistributing sediments along its entire length (De Stigter et al., 2007; Martin et al., 2011), which probably leads to resuspension and transport of coastal-neritic coccolith species from the upper canyon reaches toward the middle and lower reaches (Guerreiro et al., submitted-b; Chapter 4). On the contrary, the Lisbon-Setúbal Canyon head is located further offshore, where it is apparently less affected by coastal dynamics. Representing a calmer environment, this canyon system seems to be mainly trapping particles from vertical flux. The result of this is a relatively more pelagic sedimentation (De Stigter et al., 2011) and a (paleo)ecological signature dominated by coccoliths from oceanic species (Cl, UUR; see Figures 5.3a and 5.3e). A stronger influence of subtropical waters flowing onto this southern part of the central Portuguese margin (see Fiúza et al., 1998) should be considered to explain these coccolith assemblages. All the balances produced by CoDA revealed higher stability further offshore, i.e. the taxa within each log ratio displayed very stable proportions along that part of the W-E sections, possibly reflecting more stable depositional conditions in these deeper regions, away from littoral dynamics. Coccoliths will preferentially accumulate in fine-grained hemipelagic deposits that accumulate in more quiescent environments of the middle and lower slope, including also the lower reaches of the canyons. The resulting (paleo)ecological record expectedly appears “cleaner” offshore, i.e. less disturbed, mostly derived from vertical coccolith fluxes. On the contrary, the increasing variability of the balances towards the coast reflects the increasing effect of taphonomical processes associated to coastal dynamics, which in the case of the central Portuguese margin are mostly related to coccolith resuspension and winnowing by waves and currents, rather than dilution with other sedimentary material (Guerreiro et al., submitted-b; Chapter 4).

178 (CoDA) as a tool to study the (paleo)ecology of coccolithophores

5.6.2 Compositional vs. classical approaches

Results obtained with CoDA are in good agreement with those from conventional analysis of species percentages, despite potentially spurious correlations and biased statistical analysis associated to the latter. While avoiding the major statistical problems related to the use of percentages, by providing subcompositional coherence to our dataset, CoDA allowed to validate the existence of two main coccolithophore assemblages – one of coastal-neritic affinity, represented by Cm, Hc, Go (and to a lesser extent Cp), and another of oceanic affinity represented by Cl, UUR and Gm. Likewise, the most striking (paleo)ecological differences among the five studied sectors, i.e. canyons vs. adjacent margins, and Nazaré Canyon vs. Lisbon-Setúbal Canyon, were revealed by both compositional and classical approaches. The obtained balance-dendrograms revealed to be particularly efficient, not only in providing symmetry between the coccolithophore taxa, and thus leading to more reliable interpretations, but also in representing the most important statistical features and relationships between the taxa, their degree of dispersion and relative importance within the dataset, and their spatial distribution in the study area (Figure 5.4). This study suggests that the coccolith (paleo)ecological signal preserved in sediments of the central Portuguese margin is robust, despite the strong bottom dynamics prevailing in this region, particularly around the submarine canyons. Although similar results as obtained with ilr’s may in some cases also be found by just using percentages, which seems to be the case when the data are located close to the centre of the simplex, i.e. away from the borders, one cannot be sure of this in advance; in particular, one cannot tell when they “are close enough to the centre” and, therefore, calibration with CoDA should be a basic requirement. Results suggest that combining the two approaches might be the best option in order to take full advantage of the data set: determining the species percentages may serve as a “preview” of the data and the species relative abundances, and providing leads for the SBP, whereas using CoDA is fundamental to validate and confirm the results in a consistent framework, and to assure that all the information contained in the data set is being extracted and correctly interpreted. Despite the robust spatial trends revealed by the percentages, and confirmed by CoDA, results from regression tests revealed that there is only a weak or no linear dependence at all between the balances and the distance to the coast. This suggests that the current data set, or the study region itself, contains greater ecological and taphonomical complexity than can be resolved by basic statistical models. Further exploration of this matter is beyond the scope of the present paper, and is left as an open line for future research. Distribution patterns observed in coccolith concentrations (nanno/g) and fluxes (nanno/cm2/yr) appear to be dominated by taphonomical effects, masking the (paleo)ecological signal from the fossil record; a general decrease of nanno/g of all taxa towards the coast is mostly reflecting the increase of near-bottom sedimentary dynamics towards the coast; enhanced coccolith concentrations and fluxes in the upper canyon reaches may result from enhanced coccolithophore production in the overlying photic layer (e.g. intensification of upwelling) (ecological signal - vertical flux; Mendes et al., 2011; Guerreiro et al., submitted-a;

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Chapter 3) and/or from lateral transport of coccoliths and deposition in fine-grained canyon sediments (biostratonomical signal – lateral flux) (e.g. Oliveira et al., 2007; De Stigter et al., 2007). Given that all the taxa revealed this trend more or less equally, the second hypothesis may be the most feasible. As previously mentioned, fluxes should be carefully considered since they only take into account the effect of dilution with other particles (i.e. variations in SAR), but not the effect of other taphonomical processes, such as lateral transport, resuspension and diagenesis. This is particularly true for the upper Nazaré Canyon, which has been reported to act as a morphological trap for fine sediments in transit along the coast and shelf, and the stage of recurrent resuspension phenomena driven from intensified internal tidal activity (De Stigter et al., 2007, 2011; Oliveira et al., 2007). Likewise, one cannot be sure that enhanced coccolith fluxes of all taxa on the open slope of Estremadura spur reflect favourable conditions for phytoplankton production in this region or just overestimation of SAR due to bioturbation not accounted for in the calculation of SAR. Results suggest that sedimentary/taphonomic factors equally affect all the seven taxonomic groups, masking their ecological inter-relationship. Therefore, using coccolith species concentrations and fluxes determined from SAR appears to enhance the taphonomic effects over the ecological signal and, thus, might not be the best approach when investigating the (paleo)ecology of coccolithophores from coastal-neritic-oceanic sections, particularly in the context of submarine canyons (Guerreiro et al., submitted-b; Chapter 4) Nevertheless, the two measures might be a useful indicator for coccolithophore productivity and/or terrigenous sediment starvation, and for hydrodynamic conditions over a continental margin.

5.7. Conclusions

While avoiding the major statistical problems of dealing with percentages, CoDA allowed to validate the existence of a coastal-neritic (Hc, Go and Cp) and an oceanic assemblage (Gm, Cl, UUR), with the latter revealing a relatively higher “weight” in the studied dataset. This reflects the remarkable dominance and broad distribution of Gm in the entire investigated region, suggesting this species is better adapted to more turbulent and nutrient-rich coastal regions in comparison to other oceanic taxa such as Cl and UUR. Relatively stronger mixing of the two coccolithophore assemblages in the canyons, in comparison to the adjacent shelf and slope regions, is interpreted as reflecting the role of these major submarine valleys in exchanging water masses between coastal and oceanic regions and/or the important role of internal tides and sediment gravity flows in resuspending/transporting particles from the upper canyon reaches down to their middle and lower reaches, leading to a more homogenised sedimentary and (paleo)ecological record. The Nazaré Canyon revealed the broadest range in (paleo)ecological signature and the highest “weight” of coastal-neritic coccoliths, both in shallower and deeper regions. This seems to indicate, on the one hand, higher nutrient availability in this area resulting from the proximity of

180 (CoDA) as a tool to study the (paleo)ecology of coccolithophores the canyon head to the coast and the associated intensification of upwelling, and stronger internal tidal activity in the upper canyon; on the other hand, it may be reflecting enhanced exchange of water masses between coastal and oceanic regions occurrung along this major submarine canyon, involving the advection of living coccolithophores from oceanic to more coastal areas in the upper water masses, whereas coccoliths produced by coastal-neritic species in the upper canyon reaches may be transported down-canyon by internal tides and turbidity currents acting along the bottom of the canyon. On the contrary, the Lisbon-Setúbal Canyon reveals a (paleo)ecological signature richer in coccoliths from oceanic species (Cl, UUR), probably reflecting the more offshore position of the canyon heads, and thus representing a more stable environment mainly trapping particles from vertical flux. Higher weight of Gm in the upper reaches of the canyons, in comparison to the adjacent coastal areas, suggests this species is tracing the up-canyon flow of resuspended coccoliths from the benthic layer to the canyon head and/or the preferential onflow of more oceanic water masses through the canyons. Higher weight of the oceanic assemblage in the southern part of the study area appears to be tracing a stronger influence of ENACWst, whereas a higher weight of Gm in the northern part may be tracing a stronger influence of ENACWsp in this area. Using the species concentrations and the coccolith fluxes determined from SAR appears to enhance the taphonomic effects over the ecological signal, and therefore, might not be the best approach when investigating the (paleo)ecology of coccolithophores along coast to ocean sections, particularly in the context of a continental margin dissected by submarine canyons. Enhanced coccolith concentrations and fluxes of all taxa in the upper canyon reaches appears to result mostly from lateral transport of coccoliths and deposition within these morphological traps along with fine–grained sediment in transit along the shelf. Results obtained with isometric log ratio coordinates are in good agreement with results obtained using species percentages, despite potentially spurious correlations and biased statistical analysis associated to percentage determinations. This suggests that the coccolith (paleo)ecological signal preserved in sediments of the central Portuguese margin is robust, even in the context of the highly dynamic submarine canyons. Nevertheless, calibration with ilr’s should be a basic requirement since it cannot be sure in advance that use of percentage data will produce reliable results. Combining the two approaches should be the best compromise to take the best of our data set: determining the species percentages provides a “preview” of the data and provides the basis for the SBP, whereas CoDA appears as a fundamental tool to validate and corroborate the obtained ecological signals, and to assure that all the information contained in the data set is being extracted and correctly understood.

181

Chapter 5

Acknowledgements - This work was funded by HERMES (GOCE-CT-2005-511234) and Cd Tox-CoN (FCT-PTDC/MAR/102800/2008) projects. Multicores were collected during RV Pelagia cruises which were funded by the Netherlands Organisation for Scientific Research. Samples were prepared and analysed at NANOLAB, CEGUL. A special thanks to Henko de Stigter for supplying sample material and for textual improvements, to Marc Comas for his help with CODAPACK, and to Dr. Juan José Egozcue for fruitful discussions about compositional data analysis. The first author benefits from a PhD grant (FCT-SFRH/BD/41330/2007). V. Pawlowsky-Glahn is supported by the Spanish Ministry of Economy and Competitiveness through the project METRICS Ref. MTM2012-33236.

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Chapter 6

Synthesis and Future work

Chapter 6

Synthesis and Future Work

6.1. Synthesis

The central Portuguese margin represents a complex and diversified region in terms of oceanography, bottom topography and sedimentary dynamics. Currents and water masses of distinct origins, with different hydrological and ecological characteristics, converge into this area and seasonal variation in shelf-slope circulation is modulated by seasonal shifts in the position of the Azores high and Iceland low pressure systems, resulting in alternating upwelling and downwelling along the coast. The two major submarine canyons extending from near the shore to abyssal depth, focusing geostrophical currents and oceanic water masses, and amplifying tidal and wind-forced currents, are expected to enhance vertical water transport and exchange between coastal and oceanic regions, potentially providing a nutrient source for local phytoplankton development. Phytoplankton assemblages characteristic of the canyon setting may be preserved in sediments accumulating within the canyons and adjacentshelf and slope, but high terrigenous sediment input and strong bottom water dynamics are expected to significantly dilute and disturb the (paleo)ecological signal. Extracting the ecological signal from the sedimentary record, which particularly in the context of submarine canyons is prone to taphonomical bias, represents a major challenge for paleoenvironmental reconstructions. The present thesis presents a first attempt to address this challenge, on the basis of coccolithophores and recent coccoliths collected from the central Portuguese margin. Relevant issues discussed in the various chapters of the thesis include the present day ecology and distribution of coccolithophores in the central Portuguese margin (Chapters 2 and 4), effects of the central Portuguese canyons on the ecology of coccolithophores living in the overlying surface waters, and the potential of this group as tracer for canyon processes (Chapters 3 and 4), the dichotomy between taphonomy and ecology of coccolithophores from coastal settings (Chapters 4 and 5) and statistical approaches to perform more consistent (paleo)ecological interpretations while avoiding the statistical problems associated with the use of percentages (Chapter 5).

Ecology and distribution of coccolithophores offshore Portugal

Whereas the general biogeography and habitat characteristics of coccolithophores are relatively well-described from plankton and bottom sediment surveys, the effects of local phenomena such as coastal currents, gyres, eddies, upwelling and river runoff are often less well-known. More regional studies are required to calibrate the specific local ecological tolerances of this group, and to evaluate their potential for local paleoceanographic reconstructions. Results presented in this thesis contribute to fill this gap, using the living

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coccolithophores and sediment coccolith assemblages recorded from the central Portuguese margin. Whereas coccolithophores are often considered as a typical open ocean phytoplankton group, due to their greater species diversity and numerical contribution to open ocean phytoplankton communities (e.g. McIntyre and Bé, 1967; Winter et al., 1994; Brand, 1994; Ziveri et al., 2004), coccolithophores were found in high concentrations in coastal waters of the central Portuguese margin, exhibiting an ecological gradient from K-selected species prevailing further offshore to r-selected species occurring in higher numbers in more coastal-neritic areas. Results from the cruise in late winter 2010 reported in Chapter 2 provide a remarkable snap-shot view on the capacity of phytoplankton to rapidly respond to favourable nutrient and light conditions resulting from short-term regional meteorological and hydrographic variability Whereas surface water phytopigment data collected during this event indicate that diatoms were the dominant phytoplankton group and the main contributor of Chl-a production (data not shown), rapid exhaustion of silica by diatoms apparently worked in favour of coccolithophores which could profit from nitrates and phosphorus still available at the surface (Figures 2.6-2.7). In fact, whereas nutrient depletion from coastal waters is usually attributed to diatoms and some opportunistic dinoflagellate species (Moita, 2001; Mendes et al., 2011), the significant increase of coccolithophore cell densities observed off central Portugal in March 2010 indicates that this group can also take advantage of intermittent nutrient replenishment (Figure 2.5). Emiliania huxleyi and Gephyrocapsa oceanica were the key players of the coccolithophore bloom observed during the high-productive period of the cruise, showing a particularly rapid response to nutrient input and improved light conditions. These two species were able to compete with opportunistic small-chain diatoms, as revealed by their drastic increase of cell densities in the coastal region off Cape Carvoeiro, together with Chaetoceros s.l., Thalassiosira s.l, Skeletonema s.l., clearly confirming their role as early succession r-selected taxa, capable of rapid growth within nutrient-rich environments (Margalef, 1978). Whereas E. huxleyi did not reveal any clear distribution trend in the sediment, most likely reflecting the effects of early-diagenesis on its small-sized coccoliths closer to the coast, the coastal affinity of G. oceanica was distinctly reflected in sediments from the central Portuguese margin, particularly south of the Nazaré Canyon, where this species dominated the coccolith assemblage (Figures 4.4e and 6.1). Given its rapid response to nutrient input observed off Cape Carvoeiro, its dominance in sediments from around this area suggests that the Estremadura Spur shelf is the stage of more or less persistent high productivity. Interpretation of G. oceanica as a good (paleo)ecological proxy for enhanced productivity near the coast is in agreement with previous studies reporting the coastal ecological preference of this species (Silva et al., 2008) and its ability to quickly respond to nutrient input (Winter et al., 1994; Giraudeau and Bailey, 1995; Broerse et al., 2000; Andruleit and Rogalla, 2002; Sprengel et al., 2002; Andruleit et al., 2003). Coronosphaera mediterranea was also able to profit from favourable nutrient conditions, although less prominently than E. huxleyi and G. oceanica, and more displaced towards the shelf-break region (Figures 2.8-2.11). High cell densities in the upper water masses of the

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Nazaré Canyon head correspond well with highest coccolith percentages in the underlying sediments, suggesting persistently favourable conditions for C. mediterranea in this proximal part of the canyon (Figure 4.4b). Results confirm previous observations from Moita et al. (2010) reporting the significant occurrence of this species close to the coast off Nazaré during winter. Helicosphaera carteri also exhibited a preference for more coastal environments, correlating positively with the afore-mentioned high-productivity species during the 2nd leg of the cruise, and displaying a markedly coastal distribution within the sediment (Figures 2.11a and 4.4f). Results are in agreement with an earlier study from Guerreiro et al. (2005) reporting an extremely high percentage of H. carteri (~85 %) in sediments from the mouth of the Douro estuary, interpreted as reflecting an opportunistic behaviour possibly related with locally confined nutrient-rich conditions. On the oceanic side, Syracosphaera spp. (dominated by S. marginoporata) and Ophiaster spp. (with slightly higher densities of O. hydroideus) were the most consistently oligotrophic taxa observed in the upper photic layer during both low- and high-productive periods. Closer to the coast, the two taxa displayed a broad vertical distribution extending well below the nutrient- rich surface layer, revealing their ability to compete with E. huxleyi in the subsurface layer in these near-shore areas (Figures 2.9-2.11). This suggests that lower light and nutrient levels present in subsurface shelf waters were less limiting for these taxa than for E. huxleyi. The near absence of coccoliths from Syracosphaera spp. and Ophiaster spp. in the sediment, even in the most offshore stations, most likely reflects the lower resistance of their smaller sized-coccoliths to the effects of both biostratonomy and early-diagenesis. Instead, larger and more robust coccoliths from Calcidiscus leptoporus were consistently better represented further offshore, indicating the stronger affinity of this species for more oceanic- oligotrophic environments and its greater resistance to dissolution and breakage in comparison to the two former groups (Figure 4.4a and 6.1). C. leptoporus may therefore be considered a good proxy for coccolithophore production occurring further offshore, which is in good agreement with earlier studies reporting this species as a winter-species in Lisbon bay, tracing the advection of subtropical oceanic waters to this region (Silva et al., 2008) and, in a larger scale, associated to oceanic-oligotrophic environments, preferentially occurring within oceanic gyre centers (Ziveri et al., 2004). Gephyrocapsa ericsonii and Gephyrocapsa muellerae revealed apparently similar ecological preferences during the plankton cruise, decreasing in cell densities in shelf and upper slope waters during the high-productive period, but increasing in the most offshore waters where E. huxleyi was not significantly developing (Figure 2.11). G. muellerae was one of the most abundant placolith-bearing taxa (≥3 µm) during the low-productive period, next to E. huxleyi and G. ericsonii, with cell densities three times higher than those of G. oceanica, even at the coastal stations (Table 2.2). During the high-productive period, however, the ratio between the two species was reversed, with G. oceanica dominating over G. muellerae near the coast (see Figure 6.2a,b). In the sediment, though, G. muellerae was by far the most abundant coccolith species (≥3µm) in surface sediments, with concentrations often higher than those of

187 Chapter 6

E. huxleyi and G. ericsonii, and dominating the assemblages of both coastal and more offshore areas (except on the Estremadura shelf) (Figure 4.4d and 6.1c). Higher percentages of coccoliths from G. muellerae in sediments of oceanic areas outside the canyons are in good agreement with the relatively higher abundance of this species in more oligotrophic surface waters off central Portugal, in comparison to other placolith-bearing species such as G. oceanica, E. huxleyi). The overwhelming dominance of G. muellerae over G. oceanica in the sediment suggests that, whereas the latter may be faster and more efficient in its response to intermittent “bursts” of nutrient input, G. muellerae may maintain a more regular production on the longer run. Although phytoplankton blooms often result in higher production of zooplankton faecal pellets and therefore a more efficient transfer of coccoliths from the upper water layers to the seafloor than during non-bloom conditions (see Roth, 1994; Steinmetz, 1994; Balch, 2004), results presented here give rise to new questions about the real importance of bloom events in the generation of the sedimentary record.

Coccolithophores in the central Portuguese submarine canyons: the Nazaré and Lisbon-Setúbal canyons

Compared to the effort made over the last 15 years to characterize and understand the geology and geomorphology of the central Portuguese canyons, little was known until recently about how these canyons affect the circulation over the shelf and upper slope and the production and distribution of phytoplankton. The present thesis was specifically addressing these questions, providing some indications about the influence of the canyons on the present day ecology and distribution of coccolithophores on the central Portuguese margin. The Nazaré Canyon head appeared to be the stage of different processes converging in the near-shore area. On the one hand, this area seemed to constitute a local “pool” of oceanic water masses near the coast during winter, contrasting to nutrient-richer water masses from the surrounding shelf and coast. This was revealed by CTD sections along the upper canyon axis showing that the core of the IPC reached very near-shore areas less than 10 km off the coast via the canyon, and by the single occurrence of typical subtropical-oligotrophic species Discosphaera tubifera, Palusphaera vandelii and Calcidiscus leptoporus associated with water of southerly origin advected by the IPC (Figures 3.10d and 3.2). This observation agrees with earlier studies indicating that narrow submarine canyons may significantly deflect shelf circulation when stratification is absent (Klinck, 1988; Hickey, 1997), thereby intensifying water mass exchange between the ocean and the coast. High relative abundances of coccoliths produced by G. muellerae in sediments from the upper reaches of the Lisbon-Setúbal Canyon, and in the middle Nazaré Canyon, equivalent to abundances more typically found in the offshore areas (Figure 4.4d), could be tracing the preferential onflow of more oceanic water masses through these canyons.

188 Synthesis and Future Work

At the same time, several observations seem to support the hypothesis of enhanced phytoplankton production in the canyon head: the presence of a diverse coccolithophore assemblage dominated by the productive E. huxleyi, G. ericsonii and C. mediterranea, together with maxima of both neritic-coastal taxa (i.e. G. oceanica, Acanthoica spp.) and neritic-oceanic taxa (i.e. G. muellerae, S. dalmaticus, Alisphaera spp., Michaelsarsia elegans), and the observation of a Chl-a peak at the canyon head obtained in March 2010 (Figure 3.11c). Surface water Chl-a distribution determined from satellite data, indicate the Nazaré Canyon head as an area of persistent high phytoplankton production particularly between March and October) (Figure 3.11a). This agrees well with enhanced percentages of coastal-neritic coccolith species (C. mediterranea and H. carteri) in sediment of the canyon head in comparison to the adjacent coastal areas (Fig. 4.4b,f). Enhanced Chl-a concentrations often found south of the canyon and close to Cape Carvoeiro support previous observations by Mendes et al. (2011) of persistently high diatom concentrations south of the canyon, apparently related to intensification of upwelling along the southern canyon rim and extending its influence to the shelf south of the canyon, persisting even during relaxation of upwelling-favourable winds. The relatively higher diversity of coccolithophores found in the canyon head may be considered as representative for late-winter conditions in the upper Nazaré Canyon, involving locally enhanced production of more opportunistic phytoplankton species by upwelling intensification and internal tidal pumping, and introduction of oceanic species along with the shoreward advection of oceanic and oligotrophic water masses through the narrow upper canyon (see Figure 6.1). The more pronounced mixing of coccoliths from both coastal-neritic and oceanic species in sediments from the Nazaré Canyon, compared to the Lisbon-Setúbal Canyon, confirms the enhanced exchange of water masses between coastal and oceanic regions in the Nazaré Canyon system. This seems not only to apply to the advection of living coccolithophores from oceanic to more coastal areas in the upper water masses ((paleo)ecological record), but also to the down-canyon transport of coccoliths produced by coastal-neritic species in the upper canyon reaches, by internal tides and turbidity currents acting along the bottom of the canyon (taphonomical record). In the vicinity of Belatina Valley, in the upper Nazaré Canyon, indications for interaction of the canyon with surface water circulation and phytoplankton production consist in local maxima in surface water concentrations of nutrients, Chl-a, and coccolithophore cell densities. Maximum density gradients between the superficial buoyant plume existing during the time of the cruise and the winter mixed layer underneath, appear to reflect a significant topographic effect induced by this narrow part of the canyon on the surface circulation, generating a front between the buoyant plume and the shelf-slope waters (Figure 3.7). This agrees with previous observations from Quaresma (2012) who found that this part of the canyon acts as a water drain for the surrounding area during every low tide, potentially resulting in the concentration of particles in the surface water layer, which over time would result in local nutrient-enrichment favorable for phytoplankton growth. Earlier studies also referred to the important role of ocean currents within and above submarine canyons in funneling and trapping plankton (Macquart- Moulin and Patriti, 1996; Bosley et al., 2004; Skliris and Djenidi, 2006).

189 Chapter 6

Below the surface, the vertical density gradient existing between the surficial buoyant plume and the ENACW may have promoted the baroclinic oscillation of the water masses within the narrow canyon topography. The presence of a meander in this part of the canyon axis, blocking the flow of the internal wave, seemed to enhance the vertical oscillation (Figure 3.2). Previous observations also suggested that Belatina Valley may be a site of enhanced phytoplankton productivity, through the action of internal tidal pumping of nutrients from below the canyon rim up to the photic layer, particularly under stratified conditions prevailing during summer (e.g. Oliveira et al., 2007) Similar processes have also been reported to occur in the Monterey Canyon, California (Ryan et al., 2005; 2010). When comparing the Nazaré and the Lisbon-Setúbal canyons, differences in the coccolith assemblages between the upper reaches of the two canyons seem to reflect differences in their environmental settings and dynamics; a more coastal ecological signature (i.e. dominance of C. mediterranea, H. carteri, and to some extent also G. oceanica) in the Nazaré Canyon probably reflects the greater proximity of this canyon head to the coastline and the associated intensification of upwelling and stronger influence of coastal dynamics (see Figure 6.1). On the contrary, a more oceanic ecological signature in the Lisbon-Setúbal Canyon (i.e. dominance of G. muellerae, C. leptoporus and UUR) suggests that a generally more oceanic-pelagic environment characterised by more oligotrophic nutrient conditions is prevailing in this canyon, which may be explained by its greater distance from coastal dynamics. In addition, a stronger influence of ENACWst in the southern part of the study area will expectedly leave a clearer “oceanic ecological imprint” (i.e. C. leptoporus and UUR) in this canyon. Apart from distinct ecological conditions prevailing in the surface waters overlying the Nazaré and Lisbon-Setúbal canyons, differences in their bottom sedimentary dynamics should also be considered when interpreting differences in the coccolith assemblages; i.e. stronger effects of intermittent down-canyon gravity flows and bottom resuspension by internal tidal currents in the Nazaré Canyon, in comparison to calmer sedimentary conditions prevailing in the Lisbon-Setúbal Canyon (see Figure 6.1).

Taphonomy vs. (paleo)ecology of coccolithophores in coastal settings

Although coccolith thanatocoenoses preserved in seabed sediments may be expected to show a general correspondence with the living communities dwelling in the overlying photic layer, the correspondence is generally complicated (see Steinmetz, 1994; Roth, 1994) due to modification of the primary ecological signal by a variety of taphonomical processes integrated over several months, years, decades, centuries or even thousands of years (Figure 5.1). Complexity further increases in shallower marine environments such as continental shelves, particularly in areas where submarine canyons are deeply incising the shelf and coast, and where continental and oceanic processes interplay. Sediments in such dynamic areas will always contain an averaged paleoenvironmental signal composed of the cumulative of

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Figure 6.1– Schematic representation of the most striking environmental differences between coastal submarine canyons and adjacent coast-shelf areas, using the Nazaré Canyon as example: (a) outside the canyons the coast-ocean gradient represented by r-selected taxa near the coast, and K-selected taxa further offshore, is more distinctive in comparison to the canyon (b) where a mixture of K- and r-selected taxa is noticed in the upper canyon; focusing of oceanic water masses via the canyon results in advection of subtropical taxa towards the coast and, concurrently, enhanced nutrient pumping driven by intensified upwelling and focusing of internal tidal activity in the canyon head results in enhanced production of r-selected taxa in this area. The mixing of ecologically diverse taxa is also recorded on the seabed of the canyon and extends from the upper to the middle canyon axis, with additional contribution of coccoliths resuspended and transported down-canyon by internal tides. Green colors represent the injection of nutrients by coastal upwelling and internal tidal pumping and r-selected coccolithophores (e.g. C. mediterranea – Cm; E. huxleyi – Eh; G. oceanica – Go). Thicker green arrow in the canyon illustrates the intensification of these phenomena in the upper canyon reaches. Blue colors represent onshore advection of oceanic water masses via the canyon and entrained oceanic-oligotrophic taxa (e.g. Syracosphaera spp. – Syraco; Calcidiscus leptoporus – Cl; Discosphaera tubifera – Dtub). Coccoliths represented in the figure belong to taphonomically-resistant taxa C. leptoporus, G. oceanica, C. mediterranea.

Chapter 6 ecological and sedimentary signals, of which only the stronger leave a recognisable “imprint” in the sediment. In the studied data set from the central Portuguese margin, diversity of coccolithophores in the surface water layer appeared much higher (35 species) than that of coccoliths preserved in the sediment (18 species), illustrating the significant loss of information occurring between the moment of coccolithophore production in the photic layer and the incorporation of the coccoliths within the seafloor sediment. Post-mortem loss of information (i.e. due to biostratonomy) was particularly important for smaller and more delicate taxa such as Syracosphaera spp., Ophiaster spp., S. dalmaticus which, despite their significant concentrations in the photic layer, were found to be rare or absent in the sediment. Large placolith- (Gephyrocapsa spp., C. pelagicus, C. leptoporus), helicolith- (H. carteri), and some robust caneolith-bearing taxa (C. mediterranea and Syracosphaera pulchra) appeared less affected by early diagenesis and most likely to become part of the sediment assemblage, which agrees with earlier studies reporting these species as being the most dissolution-resistant (e.g. Steinmetz, 1994; Roth, 1994; Andruleit et al., 2003; Andruleit and Rogalla, 2002; Baumann et al., 2005). In contrast, smaller placolith- bearing taxa like E. huxleyi and G. ericsonii have been recognized as more easily affected by dissolution, reason for which their coccolith concentrations are here used as qualitative indicators for the degree of preservation of the coccolith assemblages in the sediment. Indeed, in the studied assemblages from the central Portuguese margin, the most striking difference concerns the drastic relative decrease of E. huxleyi and the important relative increase of G. muellerae. Whereas E. huxleyi showed an overwhelming dominance in the living communities from both low- and high-productive periods, other species significantly increased in the sediment, even those which showed only low concentrations in the upper photic layer. Such is the case for larger species like H. carteri, C. leptoporus and C. pelagicus (Figure 6.2). Despite of its observed ability to rapidly respond to nutrient input, and relative robustness of its coccoliths, G. oceanica appeared to be less abundant in the sediment in comparison to G. muellerae, whilst in the living assemblages observed during the cruise G. oceanica was generally the more abundant of the two species. This suggests that G. muellerae may be more productive in the long run and over a broader area off Portugal, whereas G. oceanica is mostly abundant in particularly productive areas such as the upper Nazaré canyon region and adjacent southern continental shelf. This finding raises new questions on whether coccolith assemblages preserved in the sediment are mostly formed by steady production of less conspicuous “slow” coccolithophores, or by bursts of bloom species such as G. oceanica and E. huxleyi. At the same time, given the apparently broader ecological tolerance of G. muellerae, this study suggest that this species may have lower potential as paleoenvironmental proxy in comparison to G. oceanica, which appears to be particularly well adapted to high-productive coastal environments. In addition to the effects of biostratonomy and early diagenesis, winnowing by waves and currents in more near-shore areas are additional factors adding complexity to the transformation of coccolith assemblages from coastal settings. Due to their tiny size, coccoliths are less prone to accumulate in coarse-grained deposits of the shelf and upper slope, but more likely accumulate in fine-grained hemipelagic deposits of the middle and lower slope and the canyons.

192 Synthesis and Future Work

Figure 6.2 – Relative proportions of dominant coccolithophores observed in shelf and slope waters off central Portugal in March 2010 (a, Nazaré Canyon axis, low-productive period; b, off Cape Carvoeiro, high-productive period) and of coccoliths in sediments from the central Portuguese shelf and slope (c). Species relative abundances presented in (a) and (b) are based on integration of species cell densities over the 0-110 m water depth interval, such that Inventory SpA = SpA cells/m3 (0-15m)*15 + SpA cells/m3 (15-37.5m)*22.5 + SpA cells/m3 (37.5-75m)*37.5 + SpA cells/m3 (75-110m)*35. In stations where coccolithophore concentrations were lacking for certain depth intervals, concentrations were extrapolated from adjacent stations. Greater coast-to- ocean variability in (c) is due to the indiscriminate inclusion of samples from widely different settings in the graph.

193 Chapter 6

This process appears to affect all taxa, as shown by a general decrease of coccolith concentrations towards the coast particularly evident along transects across the open shelf and slope, and a general increase of coccolith concentrations and fluxes in the upper canyon reaches in comparison to the adjacent shelf areas (Figures 4.3 and 5.3). The concentration of coccoliths along with other fine-grained material in upper canyon sediment depocenters, includes both coccoliths produced in the overlying photic layer (ecological signal – vertical flux), as well as resuspended coccoliths arriving by lateral transport (biostratonomical signal – lateral flux). Despite of all these complicating factors, two distinct coccolith assemblages could be distinguished, which seem to reflect the ecological trends from the overlying photic layer off central Portugal: a coccolith assemblage of coastal affinity primarily represented by C. mediterranea, H. carteri and G. oceanica, and another assemblage of oceanic affinity, composed of C. leptoporus, G.muellerae and UUR (Figures 4.4. and 5.3). No consistent evidence for selective transport or preservation of individual taxa was found when considering the taphonomically more resistant taxa: C. leptoporus and H. carteri, two species of comparable size and expectedly comparable degree of resistance to dissolution and physical breakage, exhibited distinct and opposite distribution patterns, unrelated to trends in sediment particle size. C. leptoporus was more abundant offshore in fine-grained sediments, whereas H. carteri was more abundant close to the shore in coarser grained sediment. Similarly, G. oceanica and C. mediterranea, two smaller and more fragile coccolith species were preferably found closer to the coast despite the stronger winnowing and destructive mechanical forces in that area. In the submarine canyons, similar trends were also recorded although somewhat levelled-out, probably reflecting interference of the ecological-oceanographic signal resulting from enhanced ecological and oceanographic processes in the surface water and the taphonomical signal resulting from the intense bottom water dynamics in the canyons. Especially in the Nazaré Canyon onshore advection of oceanic coccolithophore species through the canyon and down-canyon transport of coastal-neritic coccoliths appears to result in mixing of oceanic and coastal-neritic assemblages. Even so, locally enhanced productivity in the canyon head appears to be persistent enough to be reflected in the (paleo)ecological record preserved in the sediment (see Figure 6.1). In the Lisbon-Setúbal Canyon the (paleo)ecological record may be expected to be less disturbed and determined mostly by the vertical flux of coccoliths produced in the overlying water, due to the fact that this canyon seems to represents a less dynamic sedimentary environment in comparison to the Nazaré Canyon (De Stigter et al., 2011). Nevertheless, whereas the relative increase of coccoliths of G. muellerae observed in the upper reaches of this canyon may reflect shoreward advection of oceanic water masses through the canyon, concentration of this species by taphonomical processes should not be excluded; since abundances of G. muellerae on the adjacent Sines and Estremadura shelves are distinctly lower than in the Lisbon-Setúbal canyon, and this species was by far the most abundant (≥ 3µm) in open slope sediments, the high relative abundance in upper canyon sediments may partially reflect up-canyon displacement of coccoliths from the deeper canyon and slope, along with the overall up-canyon suspended sediment transport that seems to occur in this canyon (De Stigter et al., 2011). In conclusion, results of this study seem to indicate that despite of all the factors intervening with the deposition and preservation of coccoliths in sediments of coastal-neritic areas, leading to significant loss of the initial species diversity of the live coccolithophore assemblage, the taphonomically resistant

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coccolith taxa may be useful tracers of ecological and oceanographical processes occurring on the central Portuguese margin. It appears generally more difficult to make ecological inferences based on coccoliths preserved in the sedimentary record of canyons, due to the more complex surface circulation and stronger bottom water dynamics prevailing in these areas. Knowledge of the oceanographic processes occurring in these areas appears crucial prerequisite for the correct interpretation of the ecological signals preserved in sediments from submarine canyons.

Compositional Data Analysis: the isometric log-ratio approach

Determining species relative abundance in percentage relative to the sum of total or selected common coccoliths is a standard analytical procedure in paleoecological studies, by which ecological inter-relationships between species can be inferred independently of sediment dilution effects. However, determining percentages entails inconsistencies mostly related to the closure problem, often leading to spurious correlations between the taxa and biased statistical analysis, and thus to potentially unrealistic interpretations (Pawlowsky-Glahn and Egozcue, 2006). The Compositional Data Analysis (CoDA) approach applied in this study has the advantage that scale-invariance and subcompositional coherence are satisfied, which is essential to avoid spurious correlations. By implementing the use of isometric log- ratios, CoDA allows extracting all the information contained in data variability, thus leading to more reliable comparisons and interpretations (Buccianti, 2013). In the present study, CoDA allowed to validate the existence of two main coccolithophore assemblages, initially inferred from percentage data: one of coastal-neritic affinity, and another of oceanic affinity. The most striking (paleo)ecological differences among the five studied transects, i.e. canyons vs. adjacent margins, and Nazaré Canyon vs. Lisbon-Setúbal Canyon, were also revealed by both compositional and classical approaches. CoDa balances revealed higher stability further offshore, possibly reflecting more uniform depositional conditions away from shelf and upper canyon dynamics, where the (paleo)ecological record is less disturbed and mostly derived from vertical coccolith fluxes (Figure 5.5). In contrast, the increasing variability of the balances towards the coast reflects the increasing effect of taphonomical processes associated to coastal dynamics, mostly related to coccolith resuspension and transport by waves and currents (see Chapter 4 – Table 4.2). The higher weight of the oceanic assemblage in the studied dataset reflects the significant dominance and broad distribution of G. muellerae in the study area (Figure 5.4; see section I). CoDA also confirmed the mixing of coastal and oceanic taxa along the canyons, contrasting with the clear separation between coastal and oceanic taxa on the adjacent shelf and slope areas (Figure 5.6), reflecting the different oceanographic and sedimentary dynamics of the canyons and the open shelf and slope. The good agreement between trends observed in percentage data and trends revealed by CoDA confirms the robustness of the coccolith (paleo)ecological signal preserved in sediments of the central Portuguese margin. Nevertheless, calibration with isometric log-ratio is recommended as a basic requirement in (paleo)ecological studies, since it cannot be assured in advance that use of percentage data will produce reliable results (Pawlowsky-Glahn and Egozcue, 2006). Combining the two approaches might be the best option in order to take full advantage of the data set: the species percentages serve as a

195 Chapter 6

“preview” of the data and the species relative abundances, and providing leads for the SBP, whereas using CoDA allows validating and confirming the results in a consistent framework.

6.2. Future Work

Results presented in this thesis show that coccolithophores are valuable tracers for oceanograpic, ecological and sedimentary processes occurring on the central Portuguese margin. It was demonstrated that short-term hydrographic-meteorological variability should be taken into account when interpreting coccolith assemblages preserved in the sedimentary record of continental margin settings. In addition, new insights are provided with regards to the impact of sea bottom topography and oceanographic circulation on both ecology and taphonomy of coccolithophores, and notably the role of submarine canyons as preferential conduits for advection of oceanic water masses into more coastal areas and the down-canyon transport of suspended particles near the bottom. In the case of Belatina Valley, however, where enhanced local productivity of coccolithophores inferred from in situ measurements could not be corroborated by satellite data nor by coccoliths in the sedimentary record, validation by means of additional sampling surveys may be required, addressing the seasonal and interannual variability of phytoplankton (in general) and coccolithophores (in particular), integrated with meteorological and hydrological monitoring. Enhanced productivity at Belativa Valley may be too deep and short-lived to be detected in monthly averages of surface water Chl-a obtained by satellite. Long-term in situ observations within and outside the canyon axis should therefore be performed in future studies, in order to evaluate the spatial and temporal persistency of ecological hotspots occurring in this area; i.e. how long they exist, at the surface or deeper in the water column, and if they are actually confined to the canyon axis and its immediate vicinity, or part of a larger pattern not necessarily related to the canyon. A more complete and time-integrated understanding of the influence of the central Portuguese canyons on the seasonal production and spatial distribution of coccolithophores could be obtained by means of sediment trap moorings deployed at specific locations along the canyon (i.e. canyon head, upper-middle and middle-lower canyon transition), and at different depths along the water column (i.e. just below the photic zone but above the canyon rim, at intermediate depth, and near the bottom). Although earlier studies referred to the overprinting of the productivity signal in sediment traps by resuspended or advected particles in shallower regions (i.e. Broerse, 2000; Sprengel et al., 2002), results of the present study give confidence that ecological phenomena off central Portugal are strong and persistent enough to leave their imprint in the sediment. In fact, sediment traps would allow addressing several questions concerning the transport and sedimentation of coccoliths in the canyons. By evaluating actual fluxes of coccoliths towards the canyon seafloor, it can be assessed to what extent this flux represents export production (i.e. reflecting changes in productivity in the overlying surface waters) or has a significant component determined by lateral advection and bottom resuspension of coccoliths. Finally, for testing the application of coccoliths as proxies of paleoceanographic and paleoenvironmental changes in the Nazaré Canyon region, two long sediment cores previously collected from the north and south bank of the lower Nazaré Canyon (Koho, 2008) might offer interesting

196 Synthesis and Future Work

opportunities. Analysis of coccolith assemblages from these cores may give insight in millennial scale variations in NAO during the Holocene, its frequency and impact on the sedimentary and ecological dynamics off central Portugal. Periods characterized by a negative NAO index will expectedly be marked by increased terrigenous sediment supply to the lower canyon due to intensified canyon flushing events triggered by enhanced storm and river flooding frequency; in coccolith assemblages marked by greater diversity of oceanic species and higher percentages of reworked coastal-neritic species. Periods characterized by a positive NAO index will most likely be marked by hemipelagic sedimentation, with relatively higher proportions of oceanic coccoliths. In addition, comparing coccolith assemblages from the two contrasting sedimentary environments, the north bank being affected by spill-over of sediment gravity flows going down the canyon, and the south bank apparently only affected by continuous hemipelagic deposition, may contribute to better distinction of transport in fossil coccolith assemblages.

197

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Young, J. R, Bown P.R., 1991. An ontogenetic sequence of coccoliths from the Late Jurassic Kimmeridge Clay of England. Palaeontology 34, 843-850.

Young, J., 1994. Functions of coccoliths. In: A. Winter and W. Siesser (Eds). Coccolithophores. Cambridge University Press, Cambridge, 63-82.

Young, J. R., Bown P. R., Lees J. A. (eds) Nannotax website. International Nannoplankton Association. 21 Sept 2011. URL: http://nannotax.org.

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Young, J., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I., Østergaard, J.B., 2003. A guide to extant calcareous nannoplankton taxonomy. Journal of Nannoplankton Research, Special Issue 1, 1-125.

Young, J., Henriksen, K., 2003. Biomineralization Within Vesicles: The Calcite of Coccoliths. Reviews in Mineralogy and Geochemistry 54, 189-215.

Young J.R., Westbroek P., 1991. Genotypic variation within the coccolithophorid species Emiliania huxleyi. Marine Micropalaeontology 18, 5-23.

Zapata, M., Rodriguez, F., Garrido, J.L., 2000. Separation of chlorophylls and carotenoids from 1 marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-2 containing mobile phases. Marine Ecology Progress 195, 29-45.

Ziveri, P., Thunell, R., Rio, D., 1995. Export production of coccolithophores in an upwelling region: results from San Pedro Basin, Southern California Borderlands. Marine Micropaleontology 24, 335-358.

Ziveri, P., Broerse, A.T.C., van Hinte, J.E., Westbroeck, P. Honjo, S., 2000a. The fate of coccoliths at 48°N 21°W, northeastern Atlantic. Deep-Sea Research II 47, 1853-1875.

Ziveri, P., Rutten, A., de Lange, G.J., Thomson, J., Corselli, C., 2000b. Present-day coccolith fluxes recorded in central eastern Mediterranean sediment traps and surface sediments. Palaeogeography Palaeoclimatology Palaeoecology 158, 175-195.

Ziveri, P., Baumann, K.-H., Boeckel, B., Bollmann, J., Young, J.R., 2004. Biogeography of selected Holocene coccoliths in the Atlantic Ocean. In: H.R. Thierstein and J.R. Young (Eds). Coccolithophores - From Molecular Processes to Global Impact. Springer-Verlag, Berlin, 403-428.

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Appendix A

Taxonomy of coccolithophores

Appendix A

APPENDIX A – Taxonomy of coccolithophores

For taxonomic references, see Jordan et al. (2004)

Kingdom CHROMISTA Cavalier-Smith, 1986 Division HAPTOPHYTA Hibberd, 1972 Class PRYMNESIOPHYCEAE Hibbert, 1976 emend. Cavalier-Smith et al., 1996

Order COCCOLITHALES Schwartz, 1932 emend. Edvardsen et al., 2000 Family CALCIDISCACEAE Young and Bown, 1997 Genus Calcidiscus Kamptner, 1950 Calcidiscus leptoporus* (Murray and Blackman, 1898) Loeblich and Tappan, 1978 Genus Umbilicosphaera Lohmann, 1902 Umbilicosphaera hulburtiana Gaarder 1970 Umbilicosphaera sibogae* (Weber-van Bosse, 1901) Gaarder, 1970 Family COCCOLITHACEAE Poche, 1913 emend. Young and Bown, 1997 Genus Coccolithus Schwartz, 1894 Coccolithus pelagicus subsp. braarudii* (Gaarder, 1962) Geisen et al., 2002

Order ISOCHRYSIDALES Pascher, 1910 emend. Edvardsen and Eikrem in Edvardsen et al., 2000 Family NOELAERHABDACEAE Jerkovic, 1970 emend. Young and Bown, 1997 Genus Emiliania Hay and Mohler in Hay et al., 1967 Emiliania huxleyi *(Lohmann, 1902) Hay and Mohler, 1967 Genus Gephyrocapsa Kamptner, 1943 Gephyrocapsa ericsonii* McIntyre and Bé, 1967 Gephyrocapsa muellerae* Bréhéret, 1978 Gephyrocapsa oceanica* Kamptner, 1943

Order SYRACOSPHAERALES Hay, 1977 emend. Young et al., 2003 Family CALCIOSOLENIACEAE Kamptner 1937 Genus Calciosolenia Gran 1912; emend. Young et al. 2003 (35) Calciosolenia brasiliensis*1 (Lohmann 1919) Young in Young et al. 2003 Family RHABDOSPHAERACEAE Haeckel 1894 Genus Acanthoica Lohmann 1903; emend. Schiller 1913, Kleijne 1992 Acanthoica quattrospina Lohmann 1903 Genus Algirosphaera Schlauder 1945; emend. Norris 1984 Algirosphaera robusta (Lohmann 1902) Norris 1984 Genus Discosphaera Haeckel 1894

1 Calciosolenia brasiliensis, Syracosphaera didyma, Syracosphaera lamina, Umbellosphaera tenuis and Florisphaera profunda were only observed in the form of coccoliths * Genera and/or species that were observed as coccoliths in the sediment samples.

217 Appendix A

Discosphaera tubifera (Murray and Blackman 1898) Ostenfeld 1900 Genus Palusphaera Lecal 1966a; emend. Norris 1984 Palusphaera vandelii Lecal 1966a; emend. Norris 1984 Genus Rhabdosphaera* Haeckel 1894 Rhabdosphaera clavigera Murray and Blackman 1898 Family SYRACOSPHAERACEAE (Lohmann, 1902) Lemmermann, 1903 Genus Michaelsarsia Gran 1912; emend. Manton et al. 1984 Michaelsarsia elegans Gran 1912; emend. Manton et al. 1984 Genus Ophiaster Gran 1912; emend. Manton and Oates 1983b Ophiaster formosus Gran 1912 sensu Gaarder 1967; emend. Manton and Oates 1983b var. formosus Ophiaster hydroideus (Lohmann 1903) Lohmann 1913b; emend. Manton and Oates 1983b Ophiaster cf. reductus Manton and Oates 1983b Genus Syracosphaera Lohmann, 1902 Syracosphaera anthos (Lohmann 1912) Janin 1987 Syracosphaera amoena (Kamptner 1937) Dimiza and Triantaphyllou 2008 Syracosphaera didyma2 Kleijne and Cros 2009 Syracosphaera hirsuta Kleijne and Cros 2009 Syracosphaera lamina*2 Lecal-Schlauder 1951 Syracosphaera marginaporata Knappertsbusch 1993 Syracosphaera molicshii Schiller 1925 Syracosphaera nodosa Kamptner 1941 Syracosphaera ossa (Lecal 1966b) Loeblich Jr. and Tappan 1968 Syracosphaera pulchra* Lohmann, 1902

GENERA INCERTAE SEDIS Families with possible affinities to the Syracosphaerales Family ALISPHAERACEAE Young, Kleijne and Cros in Young et al. 2003 Genus Alisphaera Heimdal 1973; emend. Jordan and Chamberlain 1993a; Kleijne et al. 2002 Alisphaera extenta Kleijne et al. 2002 Alisphaera ordinata (Kamptner 1941) Heimdal 1973 Alisphaera pinnigera Kleijne et al. 2002 Family UMBELLOSPHAERACEAE Young and Kleijne in Young et al. 2003 (70) Genus Umbellosphaera Paasche in Markali and Paasche 1955 Umbellosphaera irregularis* Paasche in Markali and Paasche1955 Umbellosphaera tenuis2 (Kamptner 1937) Paasche in Markali and Paasche 1955 Genera with possible affinities with the Syracosphaerales Genus Coronosphaera Gaarder in Gaarder and Heimdal 1977 (71) Coronosphaera mediterranea* (Lohmann 1902) Gaarder in Gaarder and Heimdal 1977

218 Appendix A

Order ZYGODISCALES Young and Bown, 1997 Family HELICOSPHAERACEAE Black, 1971 emend. Jafar and Martini, 1975 Genus Helicosphaera Kamptner, 1954 Helicosphaera carteri var. carteri* (Wallich, 1877) Kamptner, 1954 Family PONTOSPHAERACEAE Lemmermann 1908 Genus Pontosphaera* Lohmann 1902 Genus Scyphosphaera Lohmann 1902 Scyphosphaera apsteinii* Lohmann 1902

HOLOCOCCOLITH-BEARING TAXA Family CALYPTROSPHAERACEAE Boudreaux and Hay 1969 Genus Syracolithus (Kamptner 1941) Deflandre 1952 Syracolithus dalmaticus (Kamptner 1927) Loeblich Jr. and Tappan 1966

NANNOLITH-BEARING FAMILIES Family BRAARUDOSPHAERACEAE Deflandre, 1947 Genus Braarudosphaera Deflandre, 1947 Braarudosphaera bigelowii* (Gran and Braarud, 1935) Deflandre, 1947

NANNOLITH-BEARING GENERA INCERTAE SEDIS Genus Florisphaera Okada and Honjo 1973 Florisphaera profunda var. profunda *Okada and Honjo 1973

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Appendix B

High-resolution images (SEM) of coccolithophores (and other phytoplankton groups) from the Nazaré Canyon region

HERMIONE cruise, 9 – 19 March, 2010

Appendix B

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Appendix B

APPENDIX B - High-resolution images (SEM) of coccolithophores (and other phytoplankton groups) from the Nazaré Canyon region

1 2

4 3

5 6

Figures 1- Acanthoica quattrospina (station 233-5m at 46 m) , 2 - Algirosphaera robusta (station 131-25m, at 3097 m), 3-4, Alisphaera extenta (station 132-5m), 5 - Alisphaera ordinata (station 132-5m), 6 - Alisphaera pinnigera (station 103-Bottom Nepheloid Layer (BNL), at 109 m).

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224

Appendix B

7 8

9 10

11 12

Figures 7-8 - Calcidiscus leptoporus (station 89-5m, at 40 m; station 115-50m at 224 m), 9-12 - Coronosphaera mediterranea (station 146-5m at 171 m; station 238-5m at 54 m; station 89-5m at 40 m).

225

Appendix B

226

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13 14

15 16

17 18

Figures 13-14 - Coccolithus pelagicus subsp. braarudii (station 87-25m, at 225 m; station 103-Bottom Nepheloid Layer (BNL) at 109 m); 15-18 - Emiliania huxleyi, form 1, finer and frequently multilayered coccospheres (14-16 are clearly E. huxleyi type B) (station 233-5m at 46 m; station 85-50m at 306 m; station 101-25m at 51 m; station 89-5m at 40 m) (e.g. Young and Westbroek, 1991; Young et al., 2003).

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228

Appendix B

19 20

21 22

23 24

Figures 19 – Emiliania huxleyi, form 2, (E. huxleyi type A), more calcified and robust coccospheres, in comparison with form 1 (station 95-Bottom Nepheloid Layer (BNL) at 42m); 20 - E. huxleyi, form 3 refers to E. huxleyi Type A overcalcified (station 89-5m at 40 m), 21 - Gephyrocapsa ericsonii (station 87-25m at 225 m), 22 - Gephyrocapsa muellerae (station 87-25m), 23 - Gephyrocapsa oceanica (station 87-25m), 24 – Cluster of G. oceanica (station 230- 25m at165 m).

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Appendix B

230

Appendix B

25 26

27 28

29 30

Figures 25-26 - Helicosphaera carteri var. carteri (station 87-25m at 225 m; station 95-Bottom Nepheloid Layer (BNL) at 42 m), 27-30 - Ophiaster formosus (station131-25m at 3087 m; station 132-5m at 3478 m; station 131-25m; station 115-50 m at 224 m).

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Appendix B

31 32

33 34

35 36

Figures 31 - Syracosphaera anthos (station 87-25m, at 225 m), 32 - Syracosphaera amoena (station 87-25m), 33 - Syracosphaera marginoporata (station 131-25m, at 3097 m), 34 - Syracosphaera molischii (station 96-Bottom Nepheloid Layer (BNL), at 56 m), 35 - Syracosphaera nodosa (station 103-Bottom Nepheloid Layer (BNL), at 109 m depth), 36 - Syracosphaera ossa (station 103-BNL).

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Appendix B

37 38

39 40

41 42

Figures 37 - Syracosphaera sp. (hirsuta) with an E. huxleyi on the right (station 115-50m, at 224 m depth), 38 - Syracosphaera pulchra (station 176-5m at 2024 m), 39-40 - Syracolithus dalmaticus (station 85-50m, at 306 m depth), 41 – Palusphaera vandelii (station 98-25m, at 361 m), 42 – Braarudosphaera bigelowii (station 103 - Bottom Nepheloid Layer (BNL), at 109 m).

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236

a b c

d e f Figure 43 - Some aspects of the dominant diatom groups that were often observed in the filters, especially those from off Carvoeiro cape and from the middle-lower canyon transition: a-b, chains of Thalassiosira sp., c - Skeletonema costatum, d-e, Thalassiosira sp., f- Diatoms s.l., g - Thalassionema sp., h - Chaetoceros sp., i – Diatoms s.l. g h i

Appendix

a b c

d e f

g h i

j k l

Figure 44 - a-b - Sticholonche zanclea (Radiolaria), c, - Dictyocha fibula (Silicoflagelate), d-e, Meringosphaera sp., f - Haptophyta silifera, g - Ceratium sp. (dinoflagellate), h – Radiolaria, i - Protoperidinium sp., j-k, Indetermined, l - Thoracosphaera s.l. (Calcaric dinoflagelate).

Figure 45 – General aspect of a sample collected at the Nazaré Canyon head: intact coccosphere of Emilinia huxleyi (type B) mixed with loose coccoliths (both well preserved snd reworked) and terrigenous particles (sample 85-50m, collected at 306 m depths).

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240

Figure 46 - Typical aspect of loose coccoliths from samples collected at the canyon’s head (samples 87-25m and 85-50m, at 225 m and 306 m depths, respectively). [a-h] - reworked and poorly preserved coccoliths (often belonging to larger species): (a, c) Coccolithus pelagicus, (b) Emiliania huxleyi, coccosphere partially dissolved and collapsed, (d) Umbilicosphaera sibogae, (e) Helicosphaera carteri, (f) Gephyrocapsa oceanica without bridge, (g) Calcidiscus leptoporus, (h) Coronosphaera mediterranea. [i–p] - well preserved coccoliths: (i) C. pelagicus, (j, k, n) Syracosphaera pulchra, (l) E. huxleyi, (m) H. carteri, (n) C. mediterranea, (o) Ophiaster sp., (p) U. sibogae. Scale bars: (o) =1 µm; (a-n), (p) = 2 µm.

Appendix C

Glossary and Abbreviations

Appendix

APPENDIX C - Glossary and Abbreviations

Biocoenosis (bios = life, cenosis = community) – community of organisms living in a certain region or habitat.

Biostratonomy – refers to the set of processes that are responsible for the transport of the organism’s remains from the moment of its death until the moment of its “permanent” deposition.

Bioturbation – reworking of the sediment by benthic organisms, causing horizontal and vertical displacement of sediment particles, and leading to the increase of the sediment-water interface and consequent increase of particle exchange between the sediment and the water column.

Coastal upwelling – Upward and onshore movement of cooler and denser water from deeper levels of the water column, induced by the offshore movement of the Ekman surface layer in response to longshore wind stress. Its ecological importance lies in the replenishment of surface waters with nutrients stimulating primary production.

Coastal downwelling – Downward and offshore movement of water from superficial levels of the water column, induced by the onshore movement of the Ekman surface layer in response to longshore wind stress.

Coriolis force – force apparently experienced by any object moving through a rotating reference frame, causing deflection relative to the reference frame. Winds and currents moving across the rotating Earth’s surface experience Coriolis force acting at right angles to the direction of motion, causing deflection to the right in the Northern Hemisphere and to the left on the southern Hemisphere. The Coriolis force has maximum magnitude at the poles and zero at the Equator.

Continental margin – submersed region of a continent, linking the continental landmass with the oceanic basins. It is constituted by a low-gradient and narrow continental shelf passing into a steep continental slope and rise below the shelf-break which is often located at ~150-200 m depth. Intensified exchange of water masses and organic/inorganic matter occurs between the continent and the deep-sea where submarine canyons are deeply carving the continental margin edges.

Dense water cascading – near-bottom gravity current resulting from density difference between water masses on the shelf and adjacent slope, or from denser shelf water being forced over the shelf-break by external forcing (e.g. downwelling favourable-wind), and contributing to the ventilation of intermediate and deep oceanic waters.

Diagenesis – Physical and chemical processes that lead to the alteration of the organism remains and associated mineral sedimentary component that occurs within the sedimentary matrix since after its burial.

Eastern Boundary Current – broad and shallow diffuse currents along the eastern side of oceanic basins, adjacent to the western coasts of continents (e.g. Portugal, Canary and Benguela currents on the eastern side of the Atlantic Ocean; California Current on the eastern side of Pacific Ocean). Coastal upwelling is a recurrent feature of these current systems and hence, they are highly productive.

Ekman circulation – movement of water resulting from the action of wind forcing on the ocean surface, balanced by the Coriolis force. On the Northern Hemisphere, it results in an averaged net transport of water 90º to the right of the prevailing wind direction, causing divergence (upwelling) or convergence (downwelling) of water, depending on the prevailing wind forcing direction.

Geostrophic currents – currents resulting from the balance between the Coriolis force and horizontal pressure gradients, i.e. water tends to flow from high to low pressure, as moving water tends towards a state of equilibrium, resulting in the tendency of slope and shelf currents to follow isobaths.

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Appendix

Sediment gravity flow – general term for sediment transport driven by gravity, including turbidity currents and debris flows. It results from a mixture of water and sediment particles, where the gravity acting on the sediment particles moves the fluid and not the contrary (as in land rivers), being the predominant and most efficient process by which particles are transported down a continental slope, and the prevailing transport mechanism within many submarine canyons.

Internal wave – gravity wave that oscillate within any stratified fluid medium (e.g. the atmosphere and the ocean), being commonly generated over continental margins, where stratified water flows over irregular topography. They can propagate over large distances, causing turbulence and mixing, often strong enough to resuspend bottom sediments from the shelf and slope regions and thus, contributing to the generation of bottom nepheloid layers.

Internal tide – internal waves that propagate at a tidal frequency, i.e. at diurnal and semidiurnal periods.

Necrocoenosis (necros = death; cenosis = community) – accumulation of dead organisms (dead bodies with organic matter).

Orictocoenosis (orictos = fossil; cenosis = community) – Association of fossil elements preserved in the sediment that have been subjected to diagenesis during a significant period of (geological) time.

(Paleo)biocoenosis or (paleo)ecological assemblage (paleo = old; bios = life) - community of organisms that lived in a certain biotope during a certain recent time period (i.e. not fossilized). r-selected species – species able to reproduce quickly in unstable or unpredictable, often characterized for presenting small body size and high maximum growth rates (e.g. diatoms, which are known as being opportunistic species well adapted to survive and flourish within nutrient-rich and turbulent coastal environments). As opposed to K-selected species which are better adapted to compete successfully for limited nutrient availability in more stable or predictable environments, presenting larger body size and lower maximum growth rates, resulting in very constant populations that are in equilibrium with the environmental resources (e.g. coccolithophores thriving in the subtropical oceanic gyres).

Taphocoenosis (tafos = grave; cenosis = community) – Buried association of skeletal remains within a certain sedimentation area.

Taphonomy – refers to the set of processes that rule the transition of organic remains from the biosphere towards the lithosphere, from the moment of the organism death until it is recovered as a fossil.

Thanatocoenosis (tanatos = death; cenosis = community) – Post-mortem association of skeletal remains (without organic matter) deposited on the water/sediment or subaereal/soil interfaces.

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Appendix

AC – Azores Current M – Mixing Acan – Acanthoica spp. MOW – Mediterranean Outflow Water Alisph – Alisphaera spp. NC – Nazaré Canyon B – Biostratonomy: B1, dispersion and sinking of N:P – Ratio Nitrates/ Phosphates isolated coccoliths through the water column; B2, N – Necrolysis: N1, isolated cell lysis; N2, rapid transport of coccospheres in faecal pellets zooplankton grazing towards the bottom. NAC – North Atlantic Current Biom – Biomass (Chl-a) NAO – North Atlantic Oscillation BNL – Bottom Nepheloid Layer NEADW – North East Atlantic Deep Water BP – Bouyant Plume OM – Organic Matter CC – Canary Current Ophi – Ophiaster spp. Chl-a – Chlorophyll-a P – Productivity: P1, continuous production of Cl – Calcidiscus leptoporus coccolithophores; P2, coccolithophore blooms Cm - Coronosphaera mediterranea PAR – Photossynthetic Available Radiance CoDA – Compositional Data Analysis PC – Portugal Current Corg/Ntot – Ratio between organic carbon and PMC – Particulate Matter Concentration total nitrogen PE – (Paleo)ecological Record: PEw (= weak), Cp – Coccolithus pelagicus ecological component that derives from CTD – Conductivity, Temperature, Density continuous production of coccolithophores; PEs (= strong), ecological component able to D - Diagenesis introduce changes in species inter-relationships in Dtub – Discosphaera tubifera the sedimentary record; PE’, allochtonous coccolithophore productivity (advection from Eh – Emiliania huxleyi adjacent water masses) and reworked fossil or ENACW – Eastern North Atlantic Central subfossil specimens (bottom resuspension). Water: st, subtropical origin; sp, subpolar origin; PLM – Polarizing Light Microscopy F1-F4 – Factors 1-4 from Factor Analysis SAR – Sediment Accumulation Rate FR – Fossil Record SBP – Sequential Binary Partition FTU – Formazin Turbidity Unit Sdalm – Syracolithus dalmaticus Ge – Gephyrocapsa ericsonii SEM – Scanning Electron Microscopy Gm – Gephyrocapsa muellerae Syraco – Syracosphaera spp. Go – Gephyrocapsa oceanica TS –Temperature and Salinity Hc – Helicosphaera carteri Turb - Turbidity HPLC - High-Performance Liquid UUR – Umbilicosphaera sibogae, Chromatograph Umbellosphaera irregularis, Rhabdosphaera Ilr – Isometric Log-Ratio spp. IPC – Iberian Poleward Current WIBP – Winter Iberian Bouyant Plume LDW – Lower Deep Water

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Appendix D

Digital Data

APPENDIX D – Digital Data

1 – PhD Thesis of Catarina A. Vicente Guerreiro

2 – Published paper Guerreiro, C., Oliveira, A., De Stigter, H., Cachão, M., Sá, C., Borges, C., Cros, C., Santos, A., Rodrigues, A. 2013. Late winter coccolithophore bloom off central Portugal in response to river discharge and upwelling. Continental Shelf Research 59, 65-83.

3 - List of stations from which water column samples were collected from the Nazaré Canyon region, for coccolithophore, biomass and nutrient analysis, with sampling date, position, general location, bottom depth, depth intervals for water sampling and analysis carried out. Cell densities (cells/l) of the most abundant coccolithophore species and cell counts obtained during the 1st leg (A) and 2nd leg (B) of the cruise. Stations are ordered per leg and reference.

4 – List of stations from wich surface sediment samples were collected the central Portuguese margin, for the study of recent coccolith assemblages, with coring station (mc = multicore, bc = boxcore, pc = pistoncore), position, water depth, total and individual coccolith concentrations, and number of counted coccoliths per sample, percentage of coccoliths with sizes >6 µm, between 5 and 6 µm , and between 3 and 5 µm. Sediment features previously published by De Stigter et al. (2007; 2011), Jesus et al. (2010) and Costa et al. (2011) are also presented: accumulation rate, modal and median particle -size, percentage of

CaCO3, organic material and lithogenic material, and molar Corg/Ntot ratio are also presented. Weight of each of the six isometric log-ratios (i.e. balances = β) on the studied samples (i.e. β1 [Cp, Go, Hc, Cm / Cl, UUR, Gm], (b) β2 [Cp, Go / Hc, Cm], (c) β3 [Cp / Go], (d) β4 [Hc / Cm], (e) β5 [Cl, UUR / Gm], (f) β6 [Cl / UUR]). Stations are ordered per area and reference.

251