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Tesis Doctoral On the spatial and temporal variations of zooplankton in Northeast Atlantic shelf waters Álvaro Fanjul Miranda 2018 International PhD thesis Supervisors: Dr. Fernando Villate Dr. Arantza Iriarte (c)2018 ALVARO FANJUL MIRANDA Agradecimientos / Acknowledgements Agradecimientos / Acknowledgements This work was funded by the Spanish Ministry of Economy and Competitiveness (CGL2013- 47607-R). The L4 time series is supported by the Natural Environment Research Council´s (NERC) National Capability and we would like to thank all the ship crew and scientists in providing these data. AA was also supported by NERC and the Department for Environment, Food and Rural Affairs (Grant no. NE/L003279/1) Marine Ecosystems Research Programme. Marine Scotland Science data were collected under Scottish Government Service Level Agreement ST03p. First of all, I would like to thank my supervisors Dr. Arantza Iriarte and Dr. Fernando Villate for their guidance and support during this PhD thesis. Also, to my “third supervisor” Dr. Ibon Uriarte, for his help and the time he has spent explaining me how to perform those much-needed multivariate analysis. To Dr. Matthew Spencer for allowing me to visit the School of Environmental Sciences of Liverpool and his amazing teaching skills. To the very friendly and kind people of Liverpool that made me feel at home during my stay. To Dr. Angus Atkinson and Dr. Kathryn Cook, because without their collaboration this work could not have been possible. Also, to Dr. Sergio Seoane and Dr. Aitor Laza, for sharing their experience. Finally, to Miguel Artiach for his help with polynomial orthogonal regression analyses. Me gustaría agradecer también a Fernando, “el de la zodiak”, por tener siempre una anécdota (aunque fuera repetida) para entretenerme durante las largas horas que hemos pasado bajo la lluvia y el frío. A mis amigos, los de allí, asturianos burros pero ilustrados, por todas las aventuras y desventuras que me han servido para liberar esa tensión que, en ocasiones, se acumulaba peligrosamente. Por siempre estar ahí para echar unas cañas, irnos de comida, unos cacharros, echar unas partidas a lo que sea, incluso hacer deporte (raras ocasiones) … En el fondo gente a la que odio y quiero a partes iguales, mención de honor para Pablo, pero también están Sergio, Trubo, Migueru, Nitro, Chuco, Gatico, Cefe, H8r, Casal... y demás gandalla. A los de aquí, los euskaldunes y también los acogidos en estas tierras como yo, compañeros de largas horas en la universidad. Especialmente a Estitxu y Ziortza (por orden alfabético) que me han aguantado como solo podría haberlo hecho mi madre y siempre he podido contar con ellas. A Mikel, que me ha ayudado sin pedir a cambio más que calentarme la oreja un poco y perforarme un tímpano con su risa estridente de perturbado. Imanol, Montse y demás antropólogos, por nuestras sesiones de terapia. Aize, Tanita y la gente encantadora de micro, Andoni, Aitziber, Idoia, Xabi, Leire… (calendario de comidas: lunes y miércoles), Txema y les buenes persones de biología celular, Erik, Ainara… (calendario de comidas: martes y jueves). A Theodomiro, por lo A. Fanjul bien que nos lo pasamos mientras formaste parte del “labo”. Luisma y Gorri, porque sois encantadores, mis compañeros de piso (Amaia, Alba, aunque ya no vivamos juntos… Elena e incluso Ibai), Vlatka y sus “encuentros sociales” … y a toda aquella gente que en mayor o menor medida han aportado algo a mi trabajo o a mi persona. A Nieves, por geolocalizarme y haber sido una persona cuya ayuda ha sido clave para no tirar la toalla, me has hecho seguir adelante para completar este trabajo. Además, me gustaría agradecer el haber llegado hasta aquí a mis padres, que siempre me han apoyado, aunque nunca entendieran del todo lo que era “ser un doctorando”, sin vosotros no sería quien soy. A mis abuelos, que me acompañarán siempre, a mis tíos y a mis primos. Resumiendo, muchas gracias a todos. List of publications List of publications Part of the present PhD thesis has been presented in four international conferences and published in the following scientific articles: • Fanjul, A., Villate, F., Uriarte, I., Iriarte, A., Atkinson, A., & Cook, K. (2017). Zooplankton variability at four monitoring sites of the Northeast Atlantic Shelves differing in latitude and trophic status. Journal of Plankton Research, 39(6), 891-909. https://doi.org/10.1093/plankt/fbx054. • Fanjul, A., Iriarte, A., Villate, F., Uriarte, I., Atkinson, A., & Cook, K. (2018). Zooplankton seasonality across a latitudinal gradient in the Northeast Atlantic Shelves Province. Continental Shelf Research, 160, 49-62. https://doi.org/10.1016/j.csr.2018.03.009. A. Fanjul Index Resumen I – X Thesis structure 1 General introduction 3 Hypothesis and objectives 13 Study area and sampling methodology 15 Data pretreatment 18 References 20 1. Chapter 1: Analyzing the different scales of zooplankton variability 29 1.1. Introduction 30 1.2. Methods 31 1.2.1. Data treatment 31 1.3. Results 33 1.3.1. Scales of variability 33 1.3.2. Interannual variations 36 1.3.3. Seasonal patterns 39 1.4. Discussion 45 1.4.1. Scales of variability 45 1.4.2. Interannual variations 45 1.4.3. Seasonal patterns 46 1.5. Conclusions 50 1.6. References 51 2. Chapter 2: Zooplankton seasonality and the influence of environmental factors 57 2.1 Introduction 58 2.2 Methods 59 2.2.1 Data preparation 59 2.2.2 Statistical analyses 60 2.3 Results 61 2.3.1 Seasonal patterns of zooplankton community and taxa contribution 61 2.3.2 Relationship between environmental factors and zooplankton seasonality 66 2.3.3 Year-to-year regularity in the seasonal patterns of water temperature, chlorophyll a and total zooplankton density 71 2.4 Discussion 73 2.4.1 Seasonal patterns of zooplankton community 73 2.4.2 Environmental drivers of zooplankton community seasonality 73 2.4.3 Contribution of individual taxa to shape seasonal zooplankton community patterns and the relationship between individual taxa and environmental drivers 75 2.4.4 Coherence of coastal zooplankton seasonality within marine biogeographic units 77 2.5 Conclusions 78 2.6 References 79 3. Chapter 3: Patterns and environmental drivers of zooplankton phenology changes 85 3.1. Introduction 86 3.2. Methods 87 3.2.1. Data preparation 87 3.2.2. Data analysis 87 3.3. Results 89 3.3.1. Interannual variations of environmental variables 89 3.3.2. Magnitude of the interannual variability of zooplankton T index between sites 90 3.3.3. Patterns of interannual variation of zooplankton T index and their environmental drivers 91 A. Fanjul 3.3.4. Magnitude of interannual variation of zooplankton T index by sites and seasons 99 3.4. Discussion 101 3.5. References 107 4. Chapter 4: Modelling multi-annual zooplankton variations 111 4.1. Introduction 112 4.2. Methods 113 4.2.1. Data analysis 113 4.3. Results 115 4.3.1. Environmental variables 115 4.3.2. Zooplankton community 116 4.3.3. Zooplankton taxa 123 4.4. Discussion 127 4.4.1. Zooplankton community 127 4.4.2. Zooplankton taxa taxa 130 4.4.3. Environmental variables 131 4.5. References 133 5. Chapter 5: Interacting effects of latitude, temperature, salinity, depth and distance offshore in modulating zooplankton assemblages 137 5.1. Introduction 138 5.2. Methods 139 5.2.1. Data preparation 139 5.2.2. Statistical analyses 139 5.3. Results 140 5.3.1. Zooplankton community composition 140 5.3.2. Differences in zooplankton community and environmental drivers 141 5.3.3. Relationships between taxa abundance and water temperature 143 5.4. Discussion 148 5.4.1. Zooplankton differences at coarse group level (ZG) 148 5.4.2. Zooplankton differences at copepod and cladoceran genera level (CCGen) 150 5.5. Conclusions 153 5.6. References 154 General conclusions 159 Annexes 161 Resumen Resumen El zooplancton, componente animal del plancton, está compuesto por organismos heterótrofos que viven en estado de flotación en las masas de agua, a merced de la corriente. Estos organismos pueden clasificarse de acuerdo a diversos criterios, como es su tipo de ciclo vital. Por un lado, nos encontramos aquellos organismos que pasan toda su vida viviendo en estado de flotación y formando parte del plancton, los denominados organismos holoplanctónicos. Por otro lado, están aquellos que, tras un periodo de vida planctónica, mayormente en estado larvario, pasarían a convertirse en necton o nadadores activos o a formar parte de la fauna bentónica, como organismos móviles o como organismos sésiles adheridos a algún sustrato, estos serían los organismos meroplanctónicos. Otro tipo de clasificación se realiza en torno a su tamaño, que oscila desde las pocas micras (nanoplancton o microplancton), hasta varios centímetros o incluso metros (macroplancton o megaplancton), siendo el mesozooplankton la fracción intermedia. Dicha fracción engloba a todos aquellos organismos comprendidos entre las 200 micras y los 2 centímetros, incluyendo los copépodos, grupo mayoritario del zooplancton, así como a la mayoría de larvas meroplanctónicas. Debido a su composición, el mesozooplancton es de gran relevancia en la literatura científica, siendo ampliamente muestreado en programas de monitoreo y series temporales. El zooplancton es una parte esencial de las redes tróficas marinas, siendo productores secundarios que se alimentan de fitoplancton (componente vegetal del plancton y productores primarios), haciendo de enlace trófico con organismos de niveles superiores como son los peces pelágicos. Entre otras importantes funciones de estos organismos estaría su participación en la recirculación del nitrógeno mediante su excreción y también en la bomba de carbono, ayudando al transporte de este elemento a las profundidades de los océanos mediante sus migraciones verticales. La composición y abundancia del zooplancton afecta directamente al reclutamiento de peces que dependen de ellos como fuente de alimento, las cuales pueden tener relevancia pesquera, siendo importantes recursos económicos y alimentarios para el ser humano, y cuyo estado actual, tras décadas de sobreexplotación, requiere de una cuidadosa atención, comprensión y manejo.
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