The Mediterranean Sea in the era of global change 2: 30 years of multidisciplinary study of the Ligurian Sea 9781786305862, 1786305860

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The Mediterranean Sea in the Era of Global Change 2

Series Editor Jean-Charles Pomerol

The Mediterranean Sea in the Era of Global Change 2 30 Years of Multidisciplinary Study of the Ligurian Sea

Edited by

Christophe Migon Paul Nival Antoine Sciandra

First published 2020 in Great Britain and the United States by ISTE Ltd and John Wiley & Sons, Inc.

Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the Copyright, Designs and Patents Act 1988, this publication may only be reproduced, stored or transmitted, in any form or by any means, with the prior permission in writing of the publishers, or in the case of reprographic reproduction in accordance with the terms and licenses issued by the CLA. Enquiries concerning reproduction outside these terms should be sent to the publishers at the undermentioned address: ISTE Ltd 27-37 St George’s Road London SW19 4EU UK

John Wiley & Sons, Inc. 111 River Street Hoboken, NJ 07030 USA

www.iste.co.uk

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© ISTE Ltd 2020 The rights of Christophe Migon, Paul Nival and Antoine Sciandra to be identified as the authors of this work have been asserted by them in accordance with the Copyright, Designs and Patents Act 1988. Library of Congress Control Number: 2019953805 British Library Cataloguing-in-Publication Data A CIP record for this book is available from the British Library ISBN 978-1-78630-586-2

Contents

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

ix

Chapter 1. Dissolved Organic Carbon Dynamics in the Ligurian Sea . . . . . . . . . . . . . . . . . . . . . . . . . . .

1

Chiara SANTINELLI

1.1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1.1. Why dissolved organic carbon? . . . . . . . . . . . . 1.1.2. Why dissolved organic carbon in the Ligurian Sea? 1.2. Dissolved organic carbon vertical distribution in the Ligurian Sea . . . . . . . . . . . . . . . . . . . . . . . . . 1.3. Dissolved organic carbon temporal variability at the DYFAMED station . . . . . . . . . . . . . . . . . . . . . 1.3.1. Seasonal variability in the upper 50 m . . . . . . . . 1.3.2. Dissolved organic carbon stocks (0–50 m) . . . . . . 1.4. Dissolved organic carbon surface distribution . . . . . . 1.5. Chromophoric dissolved organic matter . . . . . . . . . . 1.6. Carbon export to depth . . . . . . . . . . . . . . . . . . . . 1.6.1. Winter mixing . . . . . . . . . . . . . . . . . . . . . . . 1.6.2. Deep-water formation . . . . . . . . . . . . . . . . . . 1.6.3. Particulate organic carbon export . . . . . . . . . . . 1.7. Dissolved organic carbon stocks and fluxes . . . . . . . . 1.8. Main remarks and future directions . . . . . . . . . . . . . 1.9. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . 1.10. References . . . . . . . . . . . . . . . . . . . . . . . . . . .

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8 10 12 12 15 16 16 17 19 20 22 24 24

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Chapter 2. Dynamics and Export of Particulate Organic Carbon (POC) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

31

Beat GASSER, Scott W. FOWLER and Juan-Carlos MIQUEL

2.1. Historical developments of POC flux studies . . . . . . . . . . 2.2. POC in the Ligurian Sea . . . . . . . . . . . . . . . . . . . . . . 2.2.1. Carbon biogeochemistry . . . . . . . . . . . . . . . . . . . . 2.2.2. Export flux, key contributors and processes . . . . . . . . 2.2.3. Modeling POC dynamics . . . . . . . . . . . . . . . . . . . 2.3. Present status of POC flux and dynamics in the Ligurian Sea 2.4. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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31 35 35 42 52 54 57

Chapter 3. Zooplankton I. Micro- and Mesozooplankton . . . . . . . .

67

John DOLAN and Virginie RAYBAUD

3.1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1. Defining plankton and the different categories of plankton 3.1.2. Problems with the label zooplankton . . . . . . . . . . . . . 3.2. Ligurian zooplankton . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1. Introduction to microzooplankton and mesozooplankton . 3.2.2. Sampling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. The ciliate Strombidium sulcatum and the microzooplankton of the Ligurian Sea. . . . . . . . . . . . . . . . . . 3.3.1. Strombidium sulcatum . . . . . . . . . . . . . . . . . . . . . . 3.3.2. Characteristics of the Ligurian Sea assemblages of ciliates 3.3.3. Seasonal cycles of abundance of ciliates in coastal water . 3.3.4. Near-shore to off-shore abundance gradient of ciliates . . . 3.3.5. Seasonal variability in abundance of ciliates in off-shore waters and the depth gradient. . . . . . . . . . . . . . . . 3.3.6. Non-ciliate components of the microzooplankton of the Ligurian Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. The mesozooplankton of the Ligurian Sea and the copepod Centropages typicus as a case study . . . . . . . . . . . . . . . . . . . 3.4.1. Presentation of mesozooplankton and ecological role . . . 3.4.2. Characteristics of the Ligurian Sea assemblages of crustacean zooplankton . . . . . . . . . . . . . . . . . . . . . . . 3.4.3. Centropages typicus, a dominant copepod species in the Ligurian Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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67 67 71 73 73 75

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78 78 80 82 83

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89 89

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91

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95 99

Contents

Chapter 4. Zooplankton II. Macroplankton and Long-Term Series . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

vii

109

Paul NIVAL, Fabien LOMBARD, Janine CUZIN, Jacqueline GOY and Lars STEMMANN

4.1. Macroplankton: the large planktonic animals . . . . . . . . . . . . . . . 4.1.1. Overview of the size class . . . . . . . . . . . . . . . . . . . . . . . . 4.1.2. Mollusks (Gastropoda) . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.3. Annelids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.4. Chaetognaths . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.5. Planktonic prochordates – tunicates . . . . . . . . . . . . . . . . . . 4.1.6. Cnidarians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.7. Ctenophores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Micronekton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.1. Euphausiids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.2. Other micronekton species . . . . . . . . . . . . . . . . . . . . . . . 4.3. Zooplankton long-term series . . . . . . . . . . . . . . . . . . . . . . . . 4.3.1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.2. Zooplankton temporal trends in the Bay of Villefranche-sur-Mer as an indicator of Ligurian Sea dynamics . . . . . . . . . . . . . . . . . . 4.3.3. From local variability in plankton to global understanding and plankton community forecasts . . . . . . . . . . . . . . . . . . . . . . 4.4. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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109 109 110 112 113 114 119 124 126 126 129 131 131

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136 136

Chapter 5. Climate Change Effects on the Ligurian Sea Pelagic Ecosystem. What About Top Pelagic Predators? . . . . . . . . . . . . .

147

Maurizio WÜRTZ and Jean-Marc FROMENTIN

5.1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Top pelagic predators in the Ligurian Sea. What about species and what we know about their responses to local climate change? . . . . . . 5.2.1. Squids. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.2. Bony fishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.3. Sharks and rays . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.4. Sea turtles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.5. Marine mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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147

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148 149 152 159 161 162 164 165 166

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The Mediterranean Sea in the Era of Global Change 2

Chapter 6. A Biogeochemical Approach to Contamination of the Ligurian Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

175

Daniel COSSA, Scott W. FOWLER, Christophe MIGON, Lars-Éric HEIMBÜRGER-BOAVIDA and Aurélie DUFOUR

6.1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Trace metal contamination . . . . . . . . . . . . . . . . . . . . . 6.2.1. Impact of atmospheric deposition . . . . . . . . . . . . . . 6.2.2. Mercury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2.3. Tributyltin (TBT) . . . . . . . . . . . . . . . . . . . . . . . . 6.3. Radionuclides fluxes . . . . . . . . . . . . . . . . . . . . . . . . 6.4. Organic chemical contaminants . . . . . . . . . . . . . . . . . . 6.5. Contamination of the LS in the context of the global change 6.6. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . 6.7. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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175 177 177 179 184 185 189 193 198 199

Conclusion and Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . .

207

Acronyms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

221

Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

225

List of Authors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

243

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

245

Summary of Volume 1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

247

Preface

“Mediterranean” is a name steeped in history – cradle of civilization or a land of conflict, a surface of storms or dizzying calms. The Mediterranean is a semi-enclosed sea made up of several basins separated by straits, thresholds or only administrative boundaries. Its dynamics depend on exchanges of water, matter and also on living beings, with neighboring seas. Are these exchanges negligible or decisive in annual or long-term evolution of the Mediterranean? Within the Mediterranean, evaporation is not compensated by river inflows; as a result, increases in density, combined with decreases in temperature in winter, lead to surface waters sinking to the bottom in some areas of the Mediterranean. Outside the polar zones, this phenomenon of deep-water formation is found only in the Mediterranean where the thermohaline cell reproduces the global circulation process in miniature. For the Mediterranean basin, this results in a reverse estuarine circulation, which is characterized at Gibraltar by incoming Atlantic waters at the surface and outgoing Mediterranean waters at depth. The Atlantic water flow is therefore crucial. Its slightly salty water leaves a trace as far away as the Ligurian Sea, far from Gibraltar. However, the Atlantic flow is, above all, involved in the eastern basin in the formation of new water that will then irrigate all the regions of the Mediterranean, before mixing in specific places, into the deep water that will finally emerge in the Atlantic Ocean. Entry and exit imply a budget of non-living material, and also of living beings. As the open sea is never further than 300 km from the coast, the impact of continental inputs on pelagic areas is particularly significant. It must be taken into account that the shores of the Mediterranean are heavily populated and are the focus of important touristic, agricultural and industrial interests; continental emission sources are intense and also varied with,

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The Mediterranean Sea in the Era of Global Change 2

overall, the North responsible for anthropogenic influences and the South responsible for detritic (Saharan) natural influences. While African or European winds lift the sea, mix and carry away the surface layer, they also bring loads of matter that disrupt surface marine ecosystems. This sea, and each basin as well, appear to be the complex drivers ensuring the annual dynamics of marine ecosystems. Hydrodynamics, biology and chemistry combine locally and are subject to near or distant, rapid or long-term regulations, which are not yet fully known or predictable. For several areas of the Mediterranean Sea, knowledge has been accumulated and attempts have been made to generalize it. The Ligurian Sea is a basin in which the topography of the coasts and bottoms produces simple situations. It is an “ocean model” as described by early hydrologists. Cyclonic water circulation and central divergence result from topography. The absence of a continental shelf provides access to the deep sea, and the absence of large tides simplifies temporal dynamics. These simple conditions are the main elements of the “model”. The Ligurian Sea was a laboratory to test methods and analyze different phenomena. However, with the advent of recent apparatus and research techniques, new instruments, new research strategies and new properties have been discovered. The various examples of the dynamics of offshore ecosystems, more or less enriched by the nutrient resources stored at the sea bottom, illustrate the situations encountered in vast territories of the world ocean. The continuation and amplification of regular observations of water and planktonic populations, which began around 1895, have made it possible to identify long-term effects, particularly on a climatic scale for the entire Mediterranean basin. Knowledge about the Ligurian Sea has generally been obtained independently by laboratories, by young established researchers, during oceanographic campaigns and now, using autonomous instruments. This sea has been a training and teaching ground. The accumulation of data over time has allowed long-term series of its properties. International research programs and cooperation with other institutions have resulted in the creation of new scientific teams and large, well-equipped research vessels. It was a good opportunity to export oceanic knowledge, on the dynamics and “know-how”, capitalized in the Ligurian Sea, to the whole world. Although these snapshots on various areas are important because they are tests of hypotheses and theories, they are complementary to the exploration of all aspects of marine ecosystems, on the neighboring body of water that is easy to sample frequently, such as the Ligurian Sea. However,

Preface

xi

these distant expeditions have made it possible to define the relative place of the dynamics of the Ligurian Sea in the context of the world ocean, and to observe the amplitude of variations in the variables measured locally, with respect to those possible elsewhere. Now, the coverage capacity of all oceans with satellites and autonomous vehicles allows the continuous acquisition of new variables that must be identified and validated. The Ligurian Sea then becomes an area of testing and calibration, a kind of field laboratory giving access to the open sea. This knowledge has gradually been accumulated under various influences, within the framework of French university work, theses, master reports, or under the impetus of research agencies including CNRS, CNEXO, and also by Italian CNR, or international universities, EURATOM and IAEA. All this work and all these results deserve to be consolidated. This book is then a first step in presenting the functioning of an oceanic region, from the perspective of forming or identifying particularities and similarities with other regions of the world ocean. It also highlights the research effort that has been devoted to this part of the Mediterranean for more than 150 years. In addition to the evolution of data acquisition, we must also take into account the environmental, climatic and meteorological changes of the last three decades. Climate and meteorological changes have most likely affected the physical ocean pump. Furthermore, the supply of nutrients through external inputs has undergone significant changes, yielding modifications in plankton dynamics. A shift in phytoplankton populations in favor of species adapted to oligotrophy has indeed been observed in the Ligurian Sea. It is within this framework that the ambitions of this book are set. Christophe MIGON Paul NIVAL Antoine SCIANDRA November 2019

1 Dissolved Organic Carbon Dynamics in the Ligurian Sea

1.1. Introduction 1.1.1. Why dissolved organic carbon? Marine dissolved organic carbon (DOC), which is defined as a complex mixture of organic molecules that passes through a 0.2 µm filter, represents one of the largest (662 Pg C) [HAN 09] and the least understood reservoirs of organic carbon (C) on Earth. DOC contains as much carbon as the Earth’s atmosphere; the net oxidation of 1% of its pool would therefore introduce an amount of CO2 to the atmosphere comparable to that released by the fossil fuel burning over one year. Most DOC is autochthonous, i.e. it is produced in situ by photosynthesis and chemosynthesis and released by phytoplankton, grazers (through egestion, excretion, sloppy feeding), dissolution of particles and viral lysis (CAR15). External sources (atmosphere, rivers, groundwater and sediments) may strongly affect DOC concentration and distribution, particularly in marginal semi-enclosed basins such as the Mediterranean Sea (Med Sea). DOC also has great ecological significance as it represents the main source of energy for microbes (see Volume 1, Chapter 7 of this book series). Its consumption by heterotrophic prokaryotes fuels the microbial loop that, depending on the growth efficiency of both prokaryotic heterotrophs (BGE: bacterial growth efficiency) and their grazers, can represent a link or Chapter written by Chiara SANTINELLI.

The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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The Mediterranean Sea in the Era of Global Change 2

a sink of C for the food web. If most of the removed DOC is transformed into biomass by heterotrophic prokaryotes (high BGE), it is made available for grazers and can therefore be channeled again into the food web. If most of the removed DOC is mineralized to CO2 and inorganic nutrients (low BGE), the microbial loop represents a source of CO2 to the atmosphere and therefore a sink of C for the food web [AZA 83, FEN 08, SHE 88]. This scenario is further complicated by viruses that shift most of the energy towards the dissolved phase with modeled paradoxical effects on microbial growth, i.e. the lysis of a fraction of heterotrophic prokaryotes supports the growth of the community due to the release of labile molecules [FUH 09, FUH 99]. The oxidation of organic matter, both in its particulate and dissolved form, is responsible for oxygen consumption. Respiration is therefore tightly coupled to organic matter removal, and it is one of the major components of the carbon flux in the biosphere. Large uncertainties are associated with the estimate of respiration magnitude, as well as with our capacity to predict its response to global change. Although marine DOC is produced and removed by many different processes, its concentration always falls within a very narrow range (34–80 µM C) [CAR 10, CAR 15, HAN 09, HAN 13]. The biogeochemical feedbacks that buffer DOC concentrations are unknown, and their understanding is one of the most intriguing and pressing issues in marine science. DOC can be considered as a dynamically stable reservoir of energy for the marine ecosystem, where all the energy that escapes from the food web can accumulate and be used when and where the ecosystem needs. 1.1.1.1. Biological lability of dissolved organic carbon One of the most interesting aspects of DOC dynamics is that it includes molecules with a wide range of biological lability. Different fractions of DOC have therefore been described based on their turnover time. Labile DOC (LDOC) is defined as the fraction that is immediately used by prokaryotic heterotrophs and does not accumulate [HAN 13]. It therefore has a very low steady-state concentration, even though its production and removal rates are the highest ones. The fraction of DOC, which escapes rapid mineralization and accumulates, is considered to be recalcitrant. At least four fractions have been distinguished in this pool, depending on their lifetimes: Semi-Labile DOC (SLDOC, lifetime approximately 1.5 years), Semi-Refractory DOC (SRDOC, lifetime approximately 20 years), Refractory DOC (RDOC, lifetime 16,000 years) and Ultra-Refractory DOC

Dissolved Organic Carbon Dynamics in the Ligurian Sea

3

(URDOC, lifetime approximately 40,000 years) [HAN 13]. Deep oceanic DOC is supposed to be constituted by RDOC+URDOC; however, Follet et al. [FOL 14] support the idea that a large portion (up to 30%) of DOC in deep waters has a modern radiocarbon age and a fast turnover time, which may be supported by particle dissolution. The new idea introduced in their paper is that, when particles are mineralized, not only LDOC is released but also SLDOC and SRDOC, which can resist for months to years, explaining the modern radiocarbon of a large portion of DOC in the deep waters. 1.1.1.2. Chromophoric dissolved organic matter Chromophoric dissolved organic matter (CDOM) is the fraction of DOM that absorbs light at UV and visible wavelengths, and it represents the main factor determining the underwater light availability in open ocean and coastal waters. A fraction of CDOM also re-emits light as fluorescence and is defined as fluorescent DOM (FDOM). The absorption of the UV and blue portions of the solar radiation leads to the photodegradation of CDOM into small compounds (low molecular weight, low internal energy), with a change in its biological lability [NEL 13]. The study of the optical properties (absorption and fluorescence) of CDOM can give qualitative information on the CDOM pool, such as (1) the occurrence of different chromophores, (2) the changes in chromophores due to photodegradation and/or microbial transformation, (3) the main sources of CDOM (marine vs. terrestrial), (4) average molecular weight and aromaticity degree of CDOM and (5) biological lability; there are papers reporting that humic-like substances can be a tracer of recalcitrant DOM [CAT 15, ZHA 17], even though this is a controversial topic. 1.1.2. Why dissolved organic carbon in the Ligurian Sea? In the Med Sea, DOC shows concentrations and vertical profiles similar to the oceanic ones, with concentrations in the intermediate and deep waters equal to the lowest values found in the deep Atlantic and Pacific (36–42 μM) [SAN 15a]. The very low DOC values in the deep Med Sea were unexpected since the renewal time of deep waters in the basin is 10 times shorter (20–126 years [AND 88, ROE 91]) than the renewal time of oceanic waters. The first DOC isotope data show that DOC in Med Sea deep water has an average age of 4,500–5,100 years, 1,000 years older than in the deep Atlantic Ocean [SAN 15b]. These authors suggest that a substantial fraction (up to 45%) of what has traditionally been defined as RDOC, imported from the Atlantic Ocean to the Med Sea, can be removed on temporal scales of

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The Mediterranean Sea in the Era of Global Change 2

126 years, thereby opening intriguing questions about DOC lability and cycling in the deep Med Sea.

Figure 1.1. Map of the Ligurian Sea, with the stations (red dots) where the samples for DOC were collected in 2003 (April 28th–May 12th and September 1st–16th). The stars indicate the position of the stations where DOC data are available in the literature (Table 1.1); the dotted lines refer to the boundaries of the basin proposed by Béthoux et al. [BET 98]. The arrows represent water flows expressed in m3 yr−1 (further details are reported in Volume 1, Chapter 3 of this book series). For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

The Ligurian Sea (Figure 1.1) is characterized by cyclonic circulation, a clear stratification cycle [AND 00, VID 00] and is a site of deep-water formation [BET 83]. It is one of the areas with the highest primary production rates of the Med Sea [DOR 09, MAY 16], leading to high POC and DOC production. The continental inputs are significant only through the atmosphere (for a detailed description of the characteristics of the basin, see Volume 1, Chapter 3 of this book series). Due to its hydrology, the basin is characterized by trophic conditions varying from mesotrophy in spring to oligotrophy in summer and fall [BET 98, MAR 02b]. It can therefore be considered a natural laboratory where the major processes (i.e. thermohaline circulation, deep-water formation, seasonal cycle of stratification, intense meso- and sub-mesoscale activity, external inputs, phytoplankton seasonal cycle and composition) affecting DOC concentrations and distribution can be studied. Global change is expected to influence all the above processes (deep-water formation rates, stratification pattern, atmospheric deposition pattern and Saharan dust events) affecting both DOC cycling and the quality of DOC transferred from the atmosphere to the surface ocean, and from the surface to the dark ocean. The DYFAMED station (red star in Figure 1.1) is

Dissolved Organic Carbon Dynamics in the Ligurian Sea

5

the only open ocean site, where deep-water time series is available for DOC in the Med Sea. Due to the cyclonic circulation of the basin, this station is located in an area where vertical processes dominate over lateral advection [AND 00, BET 98]. It therefore represents an ideal site where production and removal processes and vertical export of DOC can be studied. 1.2. Dissolved organic carbon vertical distribution in the Ligurian Sea

Depth (m)

In order to summarize the present knowledge on DOC vertical distribution in the basin, all the data, collected monthly at the DYFAMED station between 1990 and 19941 [AVR 02] and [COP 93], and those collected in the Ligurian Sea in May [SAN 10] and September 2003 (Figure 1.1), were averaged by depth (Figure 1.2) and compared to all the data available for the Ligurian Sea (Table 1.1). Ligurian Sea

Ligurian Sea

Dyfamed

a) May 2003

b) September 2003

c) 1990-1994

0

0

0

-100

-100

-100

-200

-200

-200

-300

-300

-300

-400

-400

-400

-500

-500 40

50

60

70

80

90

Depth (m)

0

-500 40

50

60

70

80

90

0

40

-500

-500

-500

-1000

-1000

-1000

-1500

-1500

-1500

-2000

-2000

-2000

-2500

-2500

-2500

40 50 60 70 80 90

DOC (μM)

50

60

70

80

90

0

40 50 60 70 80 90

DOC (μM)

40 50 60 70 80 90

DOC (μM)

Figure 1.2. Vertical profiles of mean DOC, computed from all the data collected in the Ligurian Sea (red dot in Figure 1.1) in (a) May (readapted from Santinelli et al. [SAN 10]) and (b) September 2003 (unpublished data) and (c) all the data collected at the DYFAMED station between 1991 and 1994 (readapted from Avril [AVR 02]) 1 Downloaded at http://www.obs-vlfr.fr/cd_rom_dmtt/sodyf_main.htm.

6

The Mediterranean Sea in the Era of Global Change 2

These profiles also give information about the spatial variability of DOC in spring and autumn (standard deviation in Figure 1.2(a) and (b)) and the temporal variability of DOC at the DYFAMED station (standard deviation in Figure 1.2(c)). DOC vertical profiles are similar to those observed in the oceans [CAR 10, CAR 15, FON 16, HAN 13] and in the other Med Sea regions [SAN 06, SAN 10, SAN 15b]. The highest values (59–67 µM in May 2003, 69–71 µM in September 2003 and 67–82 µM at the DYFAMED station) are in the surface waters (0–100 m), and gradually decrease to reach 56–60 µM at 200 m. No subsurface maximum is observed in correspondence with deep chlorophyll maximum (DCM). This observation is in agreement with the increase in bacterial production (BP) tightly related to the peak of primary production observed at the DYFAMED station in March 2003 [BOU 09], and suggests the quick microbial removal of the LDOC released by phytoplankton. Some differences can be highlighted on the three vertical profiles. At the DYFAMED station, DOC shows the highest values with a steep decrease in the upper 200 m; below 200 m, the values keep decreasing to reach the minimum of 51 µM at 1,300 m. In contrast, when all the data collected in the Ligurian Sea are taken into account, a minimum of 42–45 µM is observed at 750–1,250 m in May 2003 and 48–49 µM at 300–750 m in September 2003. Between 1,500 and 2,000 m, the three vertical profiles show almost constant values (51–52 µM at the DYFAMED station in September 2003; 45–47 µM in May 2003). DOC slightly increases in the deep waters (>2,000 m) to reach 52–58 µM close to the bottom. Focusing on the mesopelagic and bathypelagic waters, DOC values are generally higher than in other Med Sea regions, such as the Tyrrhenian or the Ionian seas and the oceans, excluding the few values as low as 34–40 µM between 750 and 1,000 m. The high primary production, the high POC fluxes, associated with winter deep convection, can justify the high DOC concentrations at depth, which are a peculiarity of this basin. Few additional data are available for intermediate and deep (200–1,000 m) waters, and they are in the range of data reported in Figures 1.2, with the only exception being the data collected at the DYFAMED station in September 1999 when low values were observed along the entire water column (Table 1.1). Interestingly, in 1998 and 1999, very low primary production values were observed throughout the year (maximum values 500 mg C m−2 d−1) [MAR 02a].

Dissolved Organic Carbon Dynamics in the Ligurian Sea

Study area

Sampling period 1991 - 1992 Monthly 1991 - 1994 monthly

SeptemberOctober 1999

Depth (m) 0-100 1502000 2-200 2001000 10002000 0-100 100300 3001000 10002000

August DYFAMED 1999-January 0-130 2000 station 5 May 1995 30 0-50 150March 2003 500 5001000 0-50 150June 2003 500 5001000 December 2005-2006 Monthly Antares Site

0-100 Ligurian Sea

May 2003

DOC(µM) DOC Samples Reference Mean reference treatment Range ±sdt material 62-92 n.a. GF/F filter [COP 93] 50-58 55-87

82 ± 5

50-65 49-56

51 ± 2

49-81

61 ± 8

39-47

44 ± 2

37-42

39 ± 1

37-39

38 ± 1

50-113 77-95 78-102 51-62

200500 20002800

IE

GF/F filter +HgCl2

CRM

H3PO4 at 4°C

CRM

-18°C

IE 67

[AVR 02]

[SAN 12]

GF/F filter [LEM 02, VAN 01] +HgCl2

40-45 40-45 64-68

62

CRM

GF/F filter +H3PO4

[BOU 09, GHI 07]

43-47 42-45

0-40

April 2015 to 0-200 June 2016

7

CRM

39-86

CRM

50-100

68 ± 10

40-58

50 ± 4

[PUL 08]

[DJA 18]

CRM

CRM 44-60

0.2 µm filter +H3PO4 at 4°C 0.2 µm filter at -20°C 0.2 µm filter at 4°C

[SAN 10]

52 ± 4

Table 1.1. DOC concentrations reported in the literature for the Ligurian Sea. DOC range and/or mean concentration ± std are shown, depending on data availability. DOC analyses were carried out by using a Shimadzu TOC analyzer. The use of DOC reference material is indicated: n.a., not available; IE, Inter-comparison Exercise [SHA 02]; CRM, Consensus Reference Material supplied by Hansell [HAN 05]

8

The Mediterranean Sea in the Era of Global Change 2

1.3. Dissolved organic carbon temporal variability at the DYFAMED station The DOC data, collected monthly at the DYFAMED station in the years 1991–1994, represent a unique opportunity to investigate DOC seasonal cycles in the Ligurian Sea. DOC shows a clear seasonal cycle and a marked interannual variability, both in surface and deep waters (Figure 1.3).

Figure 1.3. DOC vertical distribution in the years 1991–1994 (adapted from Avril [AVR 02]). For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

Avril [AVR 02] identified a general trend with DOC distribution, physically driven during winter and biologically driven during summer and fall. In synthesis: – Mid-April to mid-June: the spring bloom period. DOC accumulates in the mixed layer because of the net DOC production by phytoplankton during spring bloom, due to the winter mixing and the consequent nutrient input from deep reservoirs.

Dissolved Organic Carbon Dynamics in the Ligurian Sea

9

– Mid-June to mid-December: the stratification period. A well-developed pycnocline forms, representing a barrier to DOC vertical transport; DOC accumulates in the mixed layer. This trend was also observed by Lemée et al. [LEM 02] between June 1999 and January 2000 in the upper 130 m. DOC accumulation is mainly explained by low removal rates. These authors observed a decrease in BP when DOC started to accumulate; interestingly, they also observed a marked increase in BGE. – Mid-December to mid-April: the winter mixing period. In this period, the DOC, accumulated and/or produced in the mixed layer, can be exported to depth, playing a crucial role in carbon export and sequestration. Some deviations with respect to this general pattern emerge from a careful analysis of the data, which would deserve a longer DOC time series to be investigated more in depth (Figure 1.3). DOC stock along the water column ranges between 1.27 and 1.39·103 g DOC m−2 in most of the studied period (mean value 1.31·103 g DOC m−2) (Figure 1.4). This indicates production and removal rates of 120 g DOC m−2 yr−1, which means that 9% of the total pool (5 µM DOC yr−1) is labile or semi-labile DOC. It is noteworthy that this value represents 77% of the mean primary production calculated at the DYFAMED site using the data collected between 1993 and 1999 [MAR 02a]. Exceptions are represented by September 1991 and March/April 1994, when values were higher than 1.40·103 g DOC m−2, and November 1991 and October/December 1992, when values were lower than 1.23·103 g DOC m−2 (Figure 1.4). Net production occurs in winter, between March and June 1993 and between May and October 1994 (Figure 1.4). Net removal did not show a clear seasonality. Mineralization rates ranged from 23.4–26.5 g DOC m−2 month−1 (1 µM DOC month−1) in 1992/1993 to 86.3–87.0 g DOC m−2 month−1 (3.6 µM DOC month−1) in 1991/1994. In March 1994, net DOC production was 142 g m−2 higher than in March 1992. In 1993 and 1994, DOC stocks did not decrease below 1.27·103 g DOC m−2, with stock 49 g DOC m−2 larger in November 1993 than in November 1992 (Figure 1.4).

10

The Mediterranean Sea in the Era of Global Change 2

Figure 1.4. DOC stocks calculated by vertical integration along the entire water column in the years 1991–1994. Green arrows refer to net production, and red −2 arrows refer to net removal. The numbers are expressed in g C m . For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

1.3.1. Seasonal variability in the upper 50 m The highest DOC concentrations and largest seasonal variability were always observed in the upper 50 m with mean values ranging between 68±4 (March 1993) and 88±6 µM (October 1991) (Figure 1.3). The maxima in mean DOC concentrations were observed in different months (October 1991, November 1992, May 1993 and April 1994), without significant differences between values (Figure 1.5). Values in autumn 1991 were significantly higher than in the following years. In March 1993, DOC reached the lowest concentration (68±4 µM). Between autumn 1991 and spring 1993, the mean values followed the same trend as the stratification index (Indexstr, calculated as the difference between density at 200 and 5 m, in agreement with Behrenfeld et al. [BEH 06]), with a maximum in September/October and a minimum in January/March (Figure 1.5). Nevertheless, a good linear correlation (DOC = 19 Indexstr + 68; R² = 0.83; p=0.01) is only observed when the data, collected between November 1992 and April 1993, are taken into account. In May 1993, when the water column began to stratify, DOC started

Dissolved Organic Carbon Dynamics in the Ligurian Sea

11

increasing; however, its peak was not observed in July 1993, when stratification was at its maximum (Indexstr = 2.11 kg m−3). Surprisingly, after July 1993, the two parameters showed an opposite trend, with the highest DOC values in April 1994, when the stratification was at its minimum (Indexstr = 0.12 kg m−3), and low value in July 1994, when stratification was at its maximum (Indexstr = 2.10 kg m−3) (Figure 1.5). Whereas DOC accumulation in well stratified surface waters is well documented both in the Med Sea and in the oceans [CAR 15, CAR 94, SAN 13], it is not easy to explain the DOC cycle in 1994, nor to understand what happened in summer 1993, which inverted the expected trend. Assuming that advection is negligible on the time scale of a few months, the 11 µM decrease in average DOC concentration in the upper 50 m between April and September 1994 can be mainly explained by microbial removal, since the water column starts to stratify, hindering DOC export below the mixed layer. These rough calculations suggest that the accumulated DOC has a turnover time of a few months and is therefore semi-labile.

Figure 1.5. Temporal trend of stratification index and mean DOC concentrations (calculated by vertical integration in the 0–50 m layer). For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

12

The Mediterranean Sea in the Era of Global Change 2

1.3.2. Dissolved organic carbon stocks (0–50 m) The DOC stocks in the upper 50 m, calculated for every month (3.42–4.41 mol DOC m−2), are higher than the stocks measured in both the Tyrrhenian (2.84–3.26 mol DOC m−2) and Adriatic Seas (2.60–3.23 mol DOC m−2) in the same layer, despite Indexstr (Figure 1.5) being lower than in the Tyrrhenian Sea (Indexstr = 0.47–3.76 kg m−3) and comparable to the Adriatic Sea (Indexstr = 0.03–0.24 kg m−3) [CAR 15, CAR 94, SAN 13]. This comparison highlights that the Ligurian Sea is characterized by a large stock of DOC in the surface layer that can be linked to an in situ production higher than in the Tyrrhenian and Adriatic Seas [LAZ 12]. The minimum is never lower than 3.42 mol DOC m−2, indicating an excess of 0.82 mol DOC m−2 in the Ligurian Sea with respect to the other basins. When the data collected in 2015–2016 [DJA 18] at the Antares site (green star in Figure 1.1) are taken into account, the 0–50 m stocks (2.9–3.5 mol m−2) are in the same range of those observed in other Med Sea regions. These authors reported that integrated DOC stock above the mixed layer had a good correspondence with the mixed layer depth (MLD) with a maximum in December when MLD was about 30 m. With the available information, it is not possible to say if these differences are due to general reduction in surface DOC stocks with time or to a high spatial variability. 1.4. Dissolved organic carbon surface distribution Focusing on the surface layer (5 m), the horizontal distribution of DOC shows high spatial variability in both May (Figure 1.6) and September 2003 (Figure 1.7), and was clearly affected by the upwelling and chlorophyll distribution. In May 2003, values ranged between 56 and 79 µM, with minima (56–60 µM) in the area affected by the upwelling, as indicated by a temperature minimum (14.9–16.0°C) and salinity maximum (Figure 1.6). Interestingly, a value as high as 79 µM is in correspondence with high chlorophyll fluorescence, even in the core of the upwelling (Figure 1.6). This observation suggests in situ production by phytoplankton through exudates. High values are also observed in the Corsica Channel and close to the Corsica coast, suggesting that both the Ligurian Current and the Western Corsican Current carry a significant amount of DOC to the Ligurian Sea.

Dissolved Organic Carbon Dynamics in the Ligurian Sea

13

Figure 1.6. Surface distribution (5 m) of DOC, chlorophyll, temperature and salinity in May 2003. Black dots refer to the sampling stations. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

September 2003 was characterized by DOC concentrations ranging between 61 and 89 µM (Figure 1.7). The lowest values are in the area affected by the upwelling (temperature, 21.2–22.9°C) as observed in May 2003, even though two peaks of 83 and 89 µM partially mask this pattern. The link with chlorophyll is less visible than in spring. The values, measured close to the DYFAMED station, were higher in May (79 µM) than in March 2003 (61 µM) and comparable in June (67 µM) and September 2003 (68 µM) [BOU 09]. These data suggest that multiple factors influence DOC distribution at the surface in the Ligurian Sea. Even though further investigation is mandatory to quantify the relative weight of these factors, a strong link between surface circulation and DOC can be highlighted. The upwelling of the Levantine Intermediate Water (LIW), characterized by a DOC minimum, dilutes DOC at the surface, on the other side, the upwelling, stimulating primary production, increases DOC in situ production. The biological lability of the released DOC determines whether it is removed quickly or whether it accumulates. The increase in DOC concentration in September, when the

14

The Mediterranean Sea in the Era of Global Change 2

surface temperature is on average 8°C higher than in May and the water column is more stratified, is explained by a decoupling between DOC production and removal. A similar result was reported by Bourguet et al. [BOU 09]; these authors observed a 5 µM increase in DOC concentration in the surface layer (0–50 m) between March and June 2003, together with a decrease in both bacterial abundance and production, indicating that DOC accumulation is mostly due to a reduction of its removal by heterotrophic prokaryotes.

Figure 1.7. Surface distribution (5 m) of DOC, chlorophyll, temperature and salinity in September 2003. Black dots refer to the sampling stations. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

Daily variation in DOC concentration and composition was also investigated at the DYFAMED station in March and June 2003 [BOU 09]. No changes in DOC concentration were observed between day and night, whereas CDOM absorbance increased during the day and biogenic dissolved lipids accumulated at night, suggesting a change in DOM composition.

Dissolved Organic Carbon Dynamics in the Ligurian Sea

15

Only one paper reports information on DOM stoichiometry in the Ligurian Sea (Antares site, green star in Figure 1.1). DOC:DON stoichiometric ratio ranged between 2 and 43 with an average value of 14±6, and DOC:DOP ranged between 326 and 2,850 with an average value of 1,227±538 [DJA 18]. 1.5. Chromophoric dissolved organic matter CDOM absorption follows a decreasing exponential law [BRI 81]. Absorption coefficients at selected wavelengths can be used as an indicator of CDOM, in addition, the spectral slope (that indicates how much fast absorption decreases at increasing wavelength) can be a proxy of photochemical processes and molecular weight [HEL 08]. In surface waters of the western Med Sea, CDOM shows higher absorption and richness in humic-like substances than in the open ocean [GAL 19, MOR 09, ORG 14]. CDOM seasonal dynamics were observed at the BOUSSOLE site (yellow star in Figure 1.1), taking into account both the absorption at 440 nm (a440) and the spectral slope between 350 and 500 nm (SCDOM) in the upper 400 m (deeper data are not available) [ORG 14]. In winter, a440 is homogeneously distributed; in spring, a subsurface maximum forms and reinforces in summer, when surface values decrease. The maxima of CDOM were observed one month later than phytoplankton bloom, mainly in correspondence with high heterotrophic bacterial abundance. In addition, the subsurface maximum was observed about 10 m above the deep chlorophyll maximum (DCM), often in correspondence with bacteria subsurface maxima, suggesting that CDOM is mainly produced by heterotrophic prokaryotes growing on phytoplankton exudates or by zooplankton [NEL 04, STE 04, XIN 14]. Yet, Organelli et al. [ORG 14] did not exclude the possibility that CDOM was produced directly by phytoplankton (e.g. [ROM 10]). Further investigation is required. The removal of CDOM from spring to summer in the surface layer was mainly ascribed to photobleaching. These authors also showed that CDOM contributes to 25–70% of total light absorbance at 440 nm in the surface layer (0-DCM) and up to 100% below the DCM [ORG 14]. No FDOM data are available for the Ligurian Sea, only surface FDOM climatology data from Argo for the whole Western basin have been shown in Organelli et al. [ORG 17].

16

The Mediterranean Sea in the Era of Global Change 2

1.6. Carbon export to depth Respiration rates are higher in the Western Mediterranean Deep Waters (WMDW) than in the deep oceans [CHR 89], but the source of energy is still elusive. Vertical fluxes of sinking particulate organic matter are not enough to support the observed respiration rates. Authors [AVR 02, COP 93, LEF 96] proposed that a substantial fraction of the energy for prokaryotic respiration in the dark ocean is supplied as DOC, exported to depth by winter mixing and deep-water formation. The observed seasonal increase in DOC concentration between 300 m and 2,000 m is evidence of DOC export to depth (Figure 1.8). DOC export down to meso and bathypelagic layers occurs by three main processes: – convective, downward winter mixing of the DOC accumulated or produced in the mixed layer [AVR 02, CAR 94, COP 93, SAN 13, SOH 05]; – transport with deep-water formation [CAR 10, SAN 10, SAN 13]; – particulate organic carbon (POC) dissolution [HEI 13, MIQ 94, TAN 02]. The DYFAMED station is an ideal site for the study of the three processes, since, due to the Ligurian frontal system and cyclonic circulation, horizontal advective movements can be overlooked [AND 00, BET 98] and a time series is available. 1.6.1. Winter mixing The estimate of DOC export below 100 m by winter mixing was possible for the first time in the Med Sea thanks to the monthly DOC data collected at the DYFAMED station in 1991 and 1992. Copin-Montégut and Avril [COP 93] estimated that 14.8 g DOC m−2 yr−1 are transported below 100 m by winter mixing processes and 3.6 g DOC m−2 yr−1 are transferred by diffusion, leading to a total flux of 18.4 g DOC m−2 yr−1. Avril [AVR 02], using a longer time series (1991–1994), estimated a flux of 10.9 g DOC m−2 yr−1. The flux was calculated as the difference between maximal (late September) and minimal (mid-March) integrated DOC in the surface waters. This author estimated, using the Fickian-like diffusion law, that an additional 1.0 g DOC m−2 yr−1 are exported due to turbulent mixing during the stratification period. The sum of these values leads to an annual DOC flux through the 100 m interface close to 12 g DOC m−2 yr−1. This calculation

Dissolved Organic Carbon Dynamics in the Ligurian Sea

17

does not take into account interannual variability. Using the same approach, a flux of 16 and 19 g DOC m−2 yr−1 can be estimated for 1991 and 1992 respectively, whereas in the following years, the calculation is complicated by a change in the DOC seasonal cycle that deserves a more in-depth analysis. These fluxes are in the range of those observed in the Sargasso Sea (4.8–16.8 g DOC m−2 yr−1) [CAR 94] and in the Adriatic Sea (15.36 g DOC m−2 yr−1) [SAN 13]. It is noteworthy that they are 6–9 fold larger than the POC flux (1.3–3.2 g POC m−2 yr−1) estimated, taking into account the data collected over seven years (1993–1999) at the same site [HEI 13, MAR 02a]. 1.6.2. Deep-water formation In order to estimate DOC export to intermediate and deep waters, DOC mean values between 300 and 2,000 m are taken into account (Figure 1.8). This layer was chosen, since once DOC arrives below 300 m, it is entrained in the LIW and even though it is mineralized to CO2, it will take time (months to years) to go back to the atmosphere. This therefore represents a short-term mechanism of C sequestration.

Figure 1.8. Temporal trend of mean DOC concentrations calculated by vertical integration between 300 and 2,000 m

18

The Mediterranean Sea in the Era of Global Change 2

A clear seasonality characterizes DOC vertical distribution below 300 m (Figure 1.8), in agreement with seasonality in POC fluxes [HEI 13] and the three-step seasonal transfer scenario proposed by Migon et al. [MIG 02] (see also Volume 1, Chapter 5 of this book series). A 5–9 µM increase in average DOC concentration was observed every year between November/December and March (Figure 1.8), i.e. in the period of winter mixing, leading to the rapid transport to a depth of 89–145 g DOC m−2 yr−1 (89 g DOC m−2 yr−1 in 1993 and 145 g DOC m−2 yr−1 in 1994). These values represent 58–103% of the 0–100 m integrated phytoplankton production measured at the DYFAMED station in 1993 (154 g C m−2 yr−1) and 1994 (140 g C m−2 yr−1) [MAR 02a]. The imbalance can be explained by an underestimation of primary production (PP), since, as reported by the authors, the method used to measure PP did not take into account the release of DOC during 14C incubation, especially in oligotrophic waters, which are supposed to be dominated by small phytoplankton whose PER is high (i.e. in PP: DOC>POC). This method could determine a 50% underestimation of PP [KAR 98] in the subtropical North Pacific Ocean and up to 44% in the Western Med Sea [MOR 01]. An additional source of DOC could be the atmosphere, in agreement with Migon et al. [MIG 02]. Only one study reports direct measurement of DOC flux from the atmosphere at Cap Ferrat in 2006 [PUL 08], with a maximum deposition rate of 1.2 mmol DOC m−2 day−1 in correspondence with strong Saharan deposition events, this input is not enough to close the budget. A slight increase (3 µM) in 300–2,000 m mean DOC concentrations can be also observed in June 1993 (Figure 1.8), two months after the phytoplankton bloom (March–April; [MAR 02a]), even though the difference is very close to the detection limit of DOC analysis, this mechanism could potentially account for an additional export of 61 g DOC m−2 yr−1. The DOC exported to depth is available to prokaryotic heterotrophs thus fueling dark respiration, as indicated by the 4–7 µM DOC decrease observed between June/July and November/December in 1991–1993 and between March and May 1994 (Figure 1.8). The high stratification degree combined with the low primary production and the insignificant POC fluxes makes the microbial removal of DOC clearly visible and allows estimation of DOC removal rates of approximately 1.3 µM month−1. Exceptions to this general pattern were observed in 1994, when a 5 µM increase in the DOC average concentration was observed and resulted in an additional export below

Dissolved Organic Carbon Dynamics in the Ligurian Sea

19

300 m of 90 g DOC m−2, compared to March 1992 and 1993. Assuming that advection can be overlooked on the temporal scale of a few months, the quick removal of the exported DOC to reach concentrations as low as 51 µM in May 1994 makes it possible to estimate a removal rate of the exported DOC of 4.5 µM month−1. The DOC removal rates are comparable to those estimated in the Adriatic Sea following deep-water formation (1.2 µM month−1) [SAN 10], but the rates are 10-fold higher than those estimated for the deep oceans. This rate is also 40 times higher than the C oxidation rates (4.4 Tg C yr−1) estimated by Electronic Transport System (ETS) in the WMDW [CHR 89]. A bacterial carbon demand (BCD) of 0.48 µM month−1 can be estimated by using BP values measured under ambient pressure by Tamburini et al. [TAM 02] and assuming a BGE of 10%. BCD should correspond to the DOC removed by heterotrophic prokaryotes, in contrast BCD is three to five times lower than the DOC removal rates estimated above. DOC cycle is very dynamic and characterized by marked interannual and seasonal variability. It is therefore expected that bacteria will reply quickly to the input of semi-labile DOC by deep-water formation and that higher BP rates will be observed soon after the input of semi-labile DOC, leading to a higher BCD. The rough comparison, with data collected in April and September 2000, by Tamburini et al. [TAM 02] indicates that the data are comparable (as order of magnitude) but the exported DOC is enough to satisfy BCD. Nevertheless, a comparison among data of DOC and bacteria, collected at the same time and with a higher temporal resolution, is mandatory in order to make a more accurate comparison. 1.6.3. Particulate organic carbon export Since the 1970s, particulate organic carbon (POC) has been considered the main player in C export [MCC 75]. In oligotrophic areas, POC represents only a small fraction of the total organic carbon and most of the sinking POC is transformed to DOC and mineralized by heterotrophic prokaryotes in the upper 1,000 m of the water column [BUE 07, MAR 87]. Tanaka and Rassoulzadegan [TAN 02] reported that in the bathypelagic layer of the Ligurian Sea, POC is probably the main mechanism by which DOC is supplied. The dissolution of POC could explain the increase in DOC concentration in deep waters when the water column is strongly stratified.

20

The Mediterranean Sea in the Era of Global Change 2

POC fluxes at the DYFAMED station are characterized by high seasonal and interannual variability. In 1987/1988, POC fluxes at 200 m ranged between 3.1 mg m−2 day−1 in August and 44 mg m−2 day−1 in February [MIQ 94]. Between 1993 and 1999, POC fluxes at 200 m ranged between 1.3 and 3.2 g m−2 yr−1 [MAR 02a]. These fluxes are markedly lower than the estimates of DOC export, suggesting that most DOC export occurs through vertical mixing or, that POC fluxes are underestimated, since the dissolution of POC to DOC could be a rapid mechanism that cannot be captured by sediment traps (see Chapter 2). In other words, the POC already dissolved in DOC cannot be measured by sediment traps. These data also suggest that not all the DOC released by POC is labile, but a fraction can accumulate in the deep water on the short temporal scale, explaining the observed increase in DOC at depth. 1.7. Dissolved organic carbon stocks and fluxes DOC stocks were estimated by multiplying the mean DOC concentration in the different layers by the volume of water in the layers (Table 1.2). The resulting total DOC stock for the Ligurian Sea is 96–116·1012 g DOC (2.17 ± 0.3·1012 g DOC in the upper 50 m). Volume (104 km3)

DOC (µM) Mean ± std

Sample (n.)

Stock (1012 g)

0-100

0.50

72 ± 10

495

4.3 ± 0.6

100-300

1.01

61 ± 7

218

7.4 ± 0.8

Depth layer (m)

300-500

0.82

54 ± 6

214

5.3 ± 0.6

500-1000

2.04

53 ± 5

206

12.9 ± 1.2

4.08

51 ± 4

328

37.7 ± 3.3

1000- bottom 12

Tot DOC Stock (10 g)

96-116

Table 1.2. DOC inventory in the Ligurian Sea. The surface area assumed for the 4 2 4 2 Ligurian Sea is 5.05·10 km (Google Earth); of this area 4.08·10 km has an 4 2 average depth of 2,500 m and 0.97·10 km has an average depth of 200 m. The mean DOC concentration is calculated taking into account all the data collected at the DYFAMED station [AVR 02] and data collected in the Ligurian Sea in May [SAN 10] and September 2003 (unpublished data)

Dissolved Organic Carbon Dynamics in the Ligurian Sea

21

Primary production, estimated for the Ligurian Sea, ranges between 86 and 232 g C m−2 yr−1 with a mean value of 156 g C m−2 yr−1 [LAZ 12, MAR 02a]. Assuming this value is valid for the whole basin, a total C fixation of 4.3–11.7·1012 g C yr−1 can be estimated. Assuming that this amount represents 65–87% of total primary production (13–35% is released as DOC) [CAR 15], this would account for a DOC production of 15.1–81.2 g C m−2 yr−1, i.e. 2.6–7.1·1012 g C yr−1 on the basin scale. BP at the DYFAMED station ranged between 11.4 (autumn) and 26.6 (spring) ng C L−1 h−1; BP decreased to 0.4 ng C L−1 h−1 below 200 m. If the values, measured under ambient pressure conditions, are taken into account, it showed an average value of 1.01 ng C L−1 h−1 between 1,000 and 2,000 m [TAM 02]. Assuming a BGE of 10%, in agreement with Tamburini et al. [TAM 03], BCD is 200–466 g C m−2 yr−1 in the upper 200 m, 28 g C m−2 yr−1 between 200 and 1,000 m and 88 g C m−2 yr−1 between 1,000 and 2,000 m. Assuming these values are valid for the entire Ligurian Sea, a total BCD of 16–29·1012 g C yr−1 can be estimated (Table 1.3). Primary production would not be enough to satisfy the BCD even though all the fixed C was released as DOC. This comparison suggests that either PP and/or BGE are underestimated or additional sources of DOC are needed. DOC (1012 g C·yr-1) Source In-situ production

2.6-7.1

River input

0.06

Atmosphere

0.04-0.08

Western Corsica Current

14.5-20.7

Sardinia Current

12.2-14.9

Sink/removal BCD (BGE 10%)

16-29

BCD (BGE 25%)

6 -12

Ligurian Current

24.5-32.2

Table 1.3. DOC budget in the Ligurian Sea

Terrestrial inputs to the basin are mainly due to small rivers, the only one that can be significant is the Arno river with a total water discharge of

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The Mediterranean Sea in the Era of Global Change 2

19.4 km3 yr−1, accounting for a DOC input of 0.06·1012 g DOC yr−1 [SAN 15a]. Atmospheric input is important for this basin [MIG 02]. Only one paper reports direct measurements of DOC input from the atmosphere to the Ligurian Sea at Cap Ferrat in 2006 indicating a flux of 0.04–1.20 mmol C m−2 day−1 [PUL 08], the highest values were associated with Saharan dust deposition events. The annual flux estimated by these authors is of 129 mmol C m−2. If this flux is multiplied by the surface area of the Ligurian Sea, this would represent an external input of DOC of 0.08·1012 g C yr−1. It is noteworthy that 42% of this flux was due to a single Saharan dust deposition event, observed between June and July 2006. At the Frioul site, an atmospheric input twofold lower (59 mmol C m−2) was estimated by Djaoudi et al. [DJA 18]. In order to estimate the role of advection in the DOC budget in the Ligurian Sea, the average annual fluxes of water (reported in Figure 1.1) are multiplied by the range of mean DOC concentration in the upper 200 m, observed in May and September 2003. Even though more data and a longer temporal scale are needed to confirm these values, this rough calculation indicates a net input of DOC of 3.3–5.9 1012 g C yr−1, i.e. comparable to the DOC produced in situ, suggesting that advection of DOC is a process that cannot be overlooked. This rough budget estimate indicates that with the available information between 10 and 16·1012 g DOC yr−1 are missing in the Ligurian Sea. A BGE of 25% would reduce the imbalance (Table 1.3). 1.8. Main remarks and future directions This chapter summarizes the present knowledge of DOC dynamics in the Ligurian Sea, including a re-assessment of its stocks and fluxes on a basin scale: – surface DOC distribution is characterized by high spatial variability mainly driven by surface circulation and phytoplankton dynamics; – a clear seasonal cycle of DOC is observed in both the surface and deep layers, with periods of net production and net removal;

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– a clear seasonal cycle of CDOM is also observed, with net production in spring and net removal in summer, mainly due to photobleaching; – DOC stock along the whole water column ranges between 1.27 and 1.39 103 g DOC m−2 in most of the studied period, indicating production and removal rates of 120 g DOC m−2 yr−1 (9% of the total pool); – DOC is the main player in C export in this area, with fluxes 10 times larger than POC; – 16–19 g DOC m−2 yr−1 are exported below 100 m due to winter mixing; – 89–145 g DOC m−2 yr−1 are exported due to deep-water formation; – marked interannual variability is also observed in both the timing of the DOC cycle and in the carbon export to depth; – the main source of DOC is in situ production, determining DOC stocks larger than in the other oligotrophic regions of the Med Sea; – surface advection may represent a relevant source of DOC to the basin. The Ligurian Sea is a good model for DOC dynamics on the global ocean scale. It shows concentrations and distributions similar to the oceanic ones and due to its characteristics, it is a natural laboratory where the impact of global change on DOC cycle can be studied and modeled, with important consequences on C export and sequestration. Time series and interdisciplinary studies, linking physical, chemical and biological processes, are crucial to investigate the link between climate and DOC cycle and the impact of climate change on the carbon export to depth. Future directions to answer unresolved questions about DOC dynamics, and to shed light on the links between DOC cycle, C export, circulation pattern, primary and secondary production and climate are: – to collect new data and integrate them with laboratory experiments, satellite information and biogeochemical numerical modeling; – to investigate the relationships between DOC dynamics (concentration and distribution) and: (1) phytoplankton dynamics and composition (2) heterotrophic prokaryotes dynamics and community composition;

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– to combine DOC measurements with measurements of optical properties (absorption and fluorescence) of CDOM, in order to gain information on DOM quality; – to investigate the application of remote observational tools (e.g. satellite; BGC-Argo; gliders, i.e. high spatial and temporal resolution) to better understand CDOM and FDOM dynamics; – to get insights into the biological lability of DOC, by using incubation experiments. 1.9. Acknowledgments I express my gratitude to Christophe Migon, Paul Nival and Antoine Sciandra for inviting me to write this chapter. This chapter benefited greatly from discussion with Fabrizio D’Ortenzio, Margherita Gonnelli, Daniel Repeta and Maurizio Ribera d’Alcalà. I would also like to thank Luciano Nannicini for DOC analysis. I thank Giancarlo Bachi, Giovanni Checcucci, Valtere Evangelista, Yuri Galletti, Elisabetta Morelli and Stefano Vestri for their help preparing the manuscript. I would particularly like to thank Emanuele Organelli for his review and for his helpful comments and suggestions, which significantly improved the earlier version of the chapter. Finally, I am grateful to Gérard Copin-Montégut and Bernard Avril who started the work on dissolved organic carbon in the Ligurian Sea, making precious data available for the scientific community. 1.10. References [AND 88] ANDRIÉ C., MERLIVAT L., “Tritium in the Western Mediterranean sea during 1981 PHYCEMED cruise”, Deep-Sea Research Part A – Oceanographic Research Papers, vol. 35, pp. 247–267, 1988. [AND 00] ANDERSEN V., PRIEUR L., “One-month study in the open NW Mediterranean Sea (DYNAPROC experiment, May 1995): overview of the hydrobiogeochemical structures and effects of wind events”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 47, pp. 397–422, 2000.

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[AVR 02] AVRIL B., “DOC dynamics in the northwestern Mediterranean Sea (DYFAMED site)”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 49, pp. 2163–2182, 2002. [AZA 83] AZAM F., FENCHEL T., FIELD J.G. et al., “The ecological role of water-column microbes in the sea”, Marine Ecology Progress Series, vol. 10, pp. 257–263, 1983. [BEH 06] BEHRENFELD M.J., O’MALLEY R.T., SIEGEL D.A. et al., “Climate-driven trends in contemporary ocean productivity”, Nature, vol. 444, pp. 752–755, 2006. [BET 83] BÉTHOUX J.-P., PRIEUR L., “Hydrologie et circulation en Méditerranée nord-occidentale”, Pétroles et Techniques, vol. 299, pp. 25–34, 1983. [BET 98] BÉTHOUX J.P., MORIN P., CHAUMERY C. et al., “Nutrients in the Mediterranean Sea, mass balance and statistical analysis of concentrations with respect to environmental change”, Marine Chemistry, vol. 63, pp. 155–169, 1998. [BOU 09] BOURGUET N., GOUTX M., GHIGLIONE J.F. et al., “Lipid biomarkers and bacterial lipase activities as indicators of organic matter and bacterial dynamics in contrasted regimes at the DYFAMED site, NW Mediterranean”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 56, pp. 1454–1469, 2009. [BRI 81] BRICAUD A., MOREL A., PRIEUR L., “Absorption by dissolved organic-matter of the sea (yellow substance) in the UV and visible domains”, Limnology and Oceanography, vol. 26, pp. 43–53, 1981. [BUE 07] BUESSELER K.O., LAMBORG C.H., BOYD P.W. et al., “Revisiting carbon flux through the ocean’s twilight zone”, Science, vol. 316, pp. 567–570, 2007. [CAR 94] CARLSON C.A., DUCKLOW H.W., MICHAELS A.F., “Annual flux of dissolved organic carbon from the euphotic zone in the northwestern Saragasso Sea”, Nature, vol. 371, pp. 405–408, 1994. [CAR 10] CARLSON C.A., HANSELL D.A., NELSON N.B. et al., “Dissolved organic carbon export and subsequent remineralization in the mesopelagic and bathypelagic realms of the North Atlantic basin”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 57, pp. 1433–1445, 2010. [CAR 15] CARLSON C.A., HANSELL D.A., “DOM sources, sinks, reactivity, and budgets”, in HANSELL D.A., CARLSON C.A. (eds), Biogeochemistry of Marine Dissolved Organic Matter, 2nd Edition, Academic Press, San Diego, 2015.

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[CAT 15] CATALÀ T.S., RECHE I., FUENTES-LEMA A. et al., “Turnover time of fluorescent dissolved organic matter in the dark global ocean”, Nature Communications, vol. 6, 5986, 2015. [CHR 89] CHRISTENSEN J.P., PACKARD T.T., DORTCH F.Q. et al., “Carbon oxidation in the deep Mediterranan sea: evidence for dissolved organic carbon source”, Global Biogeochemical Cycles, vol. 3, pp. 315–335, 1989. [COP 93] COPIN-MONTÉGUT G., AVRIL B., “Vertical distribution and temporal variation of dissolved organic carbon in the North-Western Mediterranean Sea”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 40, pp. 1963–1972, 1993. [DJA 18] DJAOUDI K., VAN WAMBEKE F., BARANI A. et al., “Atmospheric fluxes of soluble organic C, N, and P to the Mediterranean Sea: potential biogeochemical implications in the surface layer”, Progress in Oceanography, vol. 163, pp. 59–69, 2018. [DOR 09] D’ORTENZIO F., RIBERA D’ ALCALA M., “On the trophic regimes of the Mediterranean Sea: a satellite analysis”, Biogeosciences, vol. 6, pp. 139–148, 2009. [FEN 08] FENCHEL T., “The microbial loop – 25 years later”, Journal of Experimental Marine Biology and Ecology, vol. 366, pp. 99–103, 2008. [FOL 14] FOLLETT C.L., REPETA D.J., ROTHMAN D.H. et al., “Hidden cycle of dissolved organic carbon in the deep ocean”, Proceedings of the National Academy of Sciences of the United States of America, vol. 111, pp. 16706–16711, 2014. [FON 16] FONTELA M., GARCIA-IBANEZ M.I., HANSELL D.A. et al., “Dissolved organic carbon in the north Atlantic meridional overturning circulation”, Scientific Reports, vol. 6, 26931, 2016. [FUH 99] FUHRMAN J.A., “Marine viruses and their biogeochemical and ecological effects”, Nature, vol. 399, pp. 541–548, 1999. [FUH 09] FUHRMAN J.A., “Microbial community structure and its functional implications”, Nature, vol. 459, pp. 193–199, 2009. [GAL 19] GALLETTI Y., GONNELLI M., RETELLETTI S.B. et al., “DOM dynamics in open waters of the Mediterranean Sea: new insights from optical properties”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 144, pp. 95–114, 2019. [GHI 07] GHIGLIONE J.F., MEVEL G., PUJO-PAY M. et al., “Diel and seasonal variations in abundance, activity, and community structure of particle-attached and free-living bacteria in NW Mediterranean Sea”, Microbial Ecology, vol. 54, pp. 217–231, 2007.

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[HAN 05] HANSELL D.A., “Dissolved organic carbon reference material program”, Eos, Transactions American Geophysical Union, vol. 86, pp. 318–318, 2005. [HAN 09] HANSELL D.A., CARLSON C.A., REPETA D.J. et al., “Dissolved organic matter in the ocean. A controversy stimulates new insights”, Oceanography, vol. 22, pp. 202–211, 2009. [HAN 13] HANSELL D.A., “Recalcitrant dissolved organic carbon fractions”, Annual Review of Marine Science, vol. 5, pp. 421–445, 2013. [HEI 13] HEIMBÜRGER L.E., LAVIGNE H., MIGON C. et al., “Temporal variability of vertical export flux at the DYFAMED time-series station (Northwestern Mediterranean Sea)”, Progress in Oceanography, vol. 119, pp. 59–67, 2013. [HEL 08] HELMS J.R., STUBBINS A., RITCHIE J.D. et al., “Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter”, Limnology and Oceanography, vol. 53, pp. 955–969, 2008. [KAR 98] KARL D.M., HEBEL D.V., BJORKMAN K. et al., “The role of dissolved organic matter release in the productivity of the oligotrophic North Pacific Ocean”, Limnology and Oceanography, vol. 43, pp. 1270–1286, 1998. [LAZ 12] LAZZARI P., SOLIDORO C., IBELLO V. et al., “Seasonal and inter-annual variability of plankton chlorophyll and primary production in the Mediterranean Sea: a modelling approach”, Biogeosciences, vol. 9, pp. 217–233, 2012. [LEF 96] LEFÈVRE D., DENIS M., LAMBERT C.E. et al., “Is DOC the main source of organic matter remineralization in the ocean water column?”, Journal of Marine Systems, vol. 7, pp. 281–291, 1996. [LEM 02] LEMÉE R., ROCHELLE-NEWALL E., VAN WAMBEKE F. et al., “Seasonal variation of bacterial production, respiration and growth efficiency in the open NW Mediterranean Sea”, Aquatic Microbial Ecology, vol. 29, pp. 227–237, 2002. [MAR 87] MARTIN J.H., KNAUER G.A., KARL D.M. et al., “VERTEX: carbon cycling in the northeast Pacific”, Deep-Sea Research Part A – Oceanographic Research Papers, vol. 34, pp. 267–285, 1987. [MAR 02a] MARTY J.-C., CHIAVÉRINI J., “Seasonal and interannual variations in phytoplankton production at DYFAMED time-series station, northwestern Mediterranean Sea”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 49, pp. 2017–2030, 2002.

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[MAR 02b] MARTY J.C., CHIAVÉRINI J., PIZAY M.D. et al., “Seasonal and interannual dynamics of nutrients and phytoplankton pigments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999)”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 49, pp. 1965–1985, 2002. [MAY 16] MAYOT N., D’ORTENZIO F., RIBERA D’ A.M. et al., “Interannual variability of the Mediterranean trophic regimes from ocean color satellites”, Biogeosciences, vol. 13, pp. 1901–1917, 2016. [MCC 75] MCCAVE I.N., “Vertical flux of particles in the ocean”, Deep-Sea Research and Oceanographic Abstracts, vol. 22, pp. 491–502, 1975. [MIG 02] MIGON C., SANDRONI V., MARTY J.C. et al., “Transfer of atmospheric matter through the euphotic layer in the northwestern Mediterranean: seasonal pattern and driving forces”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 49, pp. 2125–2141, 2002. [MIQ 94] MIQUEL J.C., FOWLER S.W., LA ROSA J. et al., “Dynamics of the downward flux of particles and carbon in the open northwestern Mediterranean Sea”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 41, pp. 243–261, 1994. [MOR 01] MORAN X.A.G., ESTRADA M., “Short-term variability of photosynthetic parameters and particulate and dissolved primary production in the Alboran Sea (SW Mediterranean)”, Marine Ecology Progress Series, vol. 212, pp. 53–67, 2001. [MOR 09] MOREL A., GENTILI B., “A simple band ratio technique to quantify the colored dissolved and detrital organic material from ocean color remotely sensed data”, Remote Sensing of Environment, vol. 113, pp. 998–1011, 2009. [NEL 04] NELSON N.B., CARLSON C.A., STEINBERG D.K., “Production of chromophoric dissolved organic matter by Sargasso Sea microbes”, Marine Chemistry, vol. 89, pp. 273–287, 2004. [NEL 13] NELSON N.B., SIEGEL D.A., “The global distribution and dynamics of chromophoric dissolved organic matter”, Annual Review of Marine Science, vol. 5, pp. 447–476, 2013. [ORG 14] ORGANELLI E., BRICAUD A., ANTOINE D. et al., “Seasonal dynamics of light absorption by chromophoric dissolved organic matter (CDOM) in the NW Mediterranean Sea (BOUSSOLE site)”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 91, pp. 72–85, 2014.

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[ORG 17] ORGANELLI E., CLAUSTRE H., BRICAUD A. et al., “Bio-optical anomalies in the world’s oceans: an investigation on the diffuse attenuation coefficients for downward irradiance derived from Biogeochemical Argo float measurements”, Journal of Geophysical Research: Oceans, vol. 122, pp. 3543–3564, 2017. [PUL 08] PULIDO-VILLENA E., WAGENER T., GUIEU C., “Bacterial response to dust pulses in the western Mediterranean: implications for carbon cycling in the oligotrophic ocean”, Global Biogeochemical Cycles, vol. 22, GB1020, 2008. [ROE 91] ROETHER W., SCHLITZER R., “Eastern Mediterranean deep water renewal on the basis of chlorofluoromethane and tritium data”, Dynamics of Atmospheres and Oceans, vol. 15, pp. 333–354, 1991. [ROM 10] ROMERA-CASTILLO C., SARMENTO H., ALVAREZ-SALGADO X.A. et al., “Production of chromophoric dissolved organic matter by marine phytoplankton”, Limnology and Oceanography, vol. 55, pp. 446–454, 2010. [SAN 06] SANTINELLI C., MANCA B.B., GASPARINI G.P. et al., “Vertical distribution of dissolved organic carbon (DOC) in the Mediterranean Sea”, Climate Research, vol. 31, pp. 205–216, 2006. [SAN 10] SANTINELLI C., NANNICINI L., SERITTI A., “DOC dynamics in the meso and bathypelagic layers of the Mediterranean Sea”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 57, pp. 1446–1459, 2010. [SAN 12] SANTINELLI C., SEMPÉRÉ R., VAN WAMBEKE F. et al., “Organic carbon dynamics in the Mediterranean Sea: an integrated study”, Global Biogeochemical Cycles, vol. 26, GB4004, 2012. [SAN 13] SANTINELLI C., HANSELL D.A., RIBERA D’ALCALA, “Influence of stratification on marine dissolved organic carbon (DOC) dynamics: the Mediterranean Sea case”, Progress in Oceanography, vol. 119, pp. 68–77, 2013. [SAN 15a] SANTINELLI C., “DOC in the Mediterranean Sea”, in HANSELL D.A., CARLSON C.A. (eds), Biogeochemistry of Marine Dissolved Organic Matter, 2nd Edition, Academic Press, San Diego, 2015. [SAN 15b] SANTINELLI C., FOLLETT C., BROGI S.R. et al., “Carbon isotope measurements reveal unexpected cycling of dissolved organic matter in the deep Mediterranean Sea”, Marine Chemistry, vol. 177, pp. 267–277, 2015. [SHA 02] SHARP J.H., CARLSON C.A., PELTZER E.T. et al., “Final dissolved organic carbon broad community intercalibration and preliminary use of DOC reference materials”, Marine Chemistry, vol. 77, pp. 239–253, 2002. [SHE 88] SHERR E., SHERR B., “Role of microbes in pelagic food webs: a revised concept”, Limnology and Oceanography, vol. 33, pp. 1225–1227, 1988.

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[SOH 05] SOHRIN R., SEMPÉRÉ R., “Seasonal variation in total organic carbon in the northeast Atlantic in 2000–2001”, Journal of Geophysical Research: Oceans, vol. 110, C10S90, 2005. [STE 04] STEINBERG D.K., NELSON N.B., CARLSON C.A. et al., “Production of chromophoric dissolved organic matter (CDOM) in the open ocean by zooplankton and the colonial cyanobacterium Trichodesmium spp”, Marine Ecology Progress Series, vol. 267, pp. 45–56, 2004. [TAM 02] TAMBURINI C., GARCIN J., RAGOT M. et al., “Biopolymer hydrolysis and bacterial production under ambient hydrostatic pressure through a 2000m water column in the NW Mediterranean”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 49, pp. 2109–2123, 2002. [TAM 03] TAMBURINI C., GARCIN J., BIANCHI A., “Role of deep-sea bacteria in organic matter mineralization and adaptation to hydrostatic pressure conditions in the NW Mediterranean Sea”, Aquatic Microbial Ecology, vol. 32, pp. 209–218, 2003. [TAN 02] TANAKA T., RASSOULZADEGAN F., “Full-depth profile (0–2000 m) of bacteria, heterotrophic nanoflagellates and ciliates in the NW Mediterranean Sea: vertical partitioning of microbial trophic structures”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 49, pp. 2093–2107, 2002. [VAN 01] VAN WAMBEKE F., GOUTX M., STRIBY L. et al., “Bacterial dynamics during the transition from spring bloom to oligotrophy in the northwestern Mediterranean Sea: relationships with particulate detritus and dissolved organic matter”, Marine Ecology Progress Series, vol. 212, pp. 89–105, 2001. [VID 00] VIDUSSI F., MARTY J.-C., CHIAVÉRINI J., “Phytoplankton pigment variations during the transition from spring bloom to oligotrophy in the northwestern Mediterranean sea”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 47, pp. 423–445, 2000. [XIN 14] XING X.G., CLAUSTRE H., WANG H.L. et al., “Seasonal dynamics in colored dissolved organic matter in the Mediterranean Sea: patterns and drivers”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 83, pp. 93–101, 2014. [ZHA 17] ZHAO Z., GONSIOR M., LUEK J. et al., “Picocyanobacteria and deep-ocean fluorescent dissolved organic matter share similar optical properties”, Nature Communications, vol. 8, 15284, 2017.

2 Dynamics and Export of Particulate Organic Carbon (POC)

2.1. Historical developments of POC flux studies The first recorded particle flux experiments were carried out in the Ligurian Sea off the coast of Monaco by researchers at the IAEA Monaco laboratory in the mid-1970s. Initial interest in studying organic particulate fluxes was spurred by analyses of zooplankton and their particulate products (i.e. fecal pellets, molts, carcasses), which showed significantly enhanced levels of a variety of trace elements, organic compounds and radionuclides compared to concentrations in the live zooplankton producing them [CHE 75, ELD 77, FOW 77, HIG 77]. Modeling studies based on these elevated concentrations in zooplankton excreta coupled with data on sinking rates of these particulates through the water column [FOW 72, KOM 81, SMA 79] have suggested that sinking fecal pellets, in particular, could account for the rapid transport of a substantial fraction of the element, radionuclide or compound in the upper surface waters to the benthos. However, quantitative in situ field data for these sinking zooplankton particulates was needed to support the findings of the models. Hence, in early 1978, the IAEA laboratory in Monaco, with assistance from a fiberglass firm in La Turbie, France, constructed its first sediment traps for collecting and quantifying sinking particles off the coast of Monaco and at other sites in the Ligurian Sea. The traps were cylindrical (H/D = 2.5; collecting area = 0.076 m2), with a conical device attached at the bottom for funneling the particles into Chapter written by Beat GASSER, Scott W. FOWLER and Juan-Carlos MIQUEL. The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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detachable polyethylene sample cups. The trap itself was made of polyester resin fiberglass covered with a gel-coat, and the collection cup was opened and closed manually with nylon cords when the trap was just beneath the surface. The first mooring deployment took place in June 1978 at a station approximately 2 km off the coast of Monaco (43°42.57’N, 7°27.30’E). The traps were deployed below the photic zone and mixed layer, at 100 m depth, in a water column approximately 225 m deep. These deployments continued periodically through July 1982. After that time, the mooring was moved further offshore to a depth of 300 m, so that additional traps at 50 m, 150 m and 250 m could be attached to the mooring to measure variation in particle flux with depth. These seasonal time-series experiments were carried out on a nearly continuous basis (weather and available ship-time permitting) until June 1984, with most of the sampling gaps occurring in winter. Nevertheless, the total carbon flux record from all those deployments represented the longest such dataset for the Mediterranean Sea at that time [FOW 91]. The first particle flux results from the June to October 1978 deployments showed that the collector samples were composed almost entirely of intact fecal pellets and gray-green amorphous flocculent matter that closely resembled descriptions of “marine snow”. Furthermore, the flocculent matter was very similar to the contents of the fecal pellets in the trapped sample. Based on computed particulate mass fluxes and measured concentrations of polychlorinated biphenyls (PCBs) in the sinking particles and copepod fecal pellets, the first data on particulate PCB vertical fluxes were reported, which supported the hypothesis that sinking zooplankton fecal pellets were the principal conveyor of these contaminants in the upper 100 m water column to depth in the Ligurian Sea ([FOW 79], see Chapter 6). Subsequent measurements during the six years of deployments demonstrated that mass and total carbon fluxes through 100 m and 150 m were maximum in winter and spring and minimum in late summer. Furthermore, it was estimated that approximately 5% of the mass flux was particulate organic carbon (POC), which resulted in POC export values out of the euphotic zone ranging from 17 to 42% of the primary production reported for this coastal region [FOW 91]. It was also shown that fecal pellet carbon flux was linearly related to the total particulate carbon flux at 50 m, 100 m and 250 m depths. Moreover, higher pellet fluxes were always found at greater depths, and calculations indicated that these pellet fluxes were approximately 25, 29 and 33% of the total particulate carbon fluxes at those depths, respectively. These early measurements clearly demonstrated that fecal pellet deposition

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can be a significant contributor to the downward particulate carbon flux in this coastal area of the Ligurian Sea.

Figure 2.1. Two types of sediment traps, PPS 3 (left) and PPS 5 (right) with a 2 2 collection surface area of 0.125 m and 1 m respectively. Also shown is some essential accessory equipment. Two pairs of four floats (left), which are used to make a fixed mooring positively buoyant for recovery. A honeycomb baffle (right) at the trap mouth to optimize trapping efficiency and prevent large organisms from entering the trap. The hexagonal honeycomb cells measure approximately 1 cm in diameter and reduce turbulence. At the bottom of the trap (right) appears the dark colored cylindrical motor that rotates the carousel with the sampling bottles. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

From these early pioneering field studies, in the following years, the development and use of sediment trap technology expanded at a rapid pace. Based on the same simple conical design, trap size increased and the collection mechanisms became more sophisticated (Figure 2.1). Paired traps were often used at each depth and were equipped with automated and electronically programmed opening and closing collection cups that would remain beneath the trap cone to collect particles for a pre-determined period of time. These developments allowed the mooring the traps at far greater depths and leaving them in place for longer periods of time, which were determined based on ship-time availability. Due to their versatility and the

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amount of particulates they could collect for the various purposes of researchers, several national and international programs and projects centered around sediment trap technology for measuring particle, carbon and contaminant fluxes were spawned in the western Mediterranean, for example DYFAMED, ECOMARGE, EROS-2000, AIRWIN, and MedFlux among others. Of those, the French DYFAMED program has been particularly important for studies in the open northwestern Mediterranean, due to its continuity and long-term status [BUA 93]. The early driving force for the DYFAMED program was the Chernobyl accident in late April 1986. By chance, a time-series experiment was carried out in the Ligurian Sea between April 13 and May 21, 1986 in which an automated time-series sediment trap was moored at a depth of 200 m in a 2,200 m water column approximately 15 nautical miles off the coast of Calvi, Corsica (42°43.9’N 8°31.3’E). Each collector cup containing a buffered preservative was programmed to collect sinking particles for consecutive periods of 6.25 days. Atmospheric measurements made at the Monaco laboratory indicated a maximum in fallout reached the sea surface in this region during 4–5 May [WHI 88]. Subsequent radio analysis of the trap samples detected radioactivity first arriving at 200 m between 2–8 May with the main pulse of particulate radionuclides arriving at that depth between 8–15 May, on average seven days after reaching the sea surface [FOW 87]. Far less or non-detectable amounts were measured in the last trap sample collected after 15 May, a time lag that implied an average sinking rate of approximately 29 m d–1. Examination of the trap samples from that period indicated that a large fraction of the sinking particles were intact zooplankton fecal pellets, which demonstrated the importance of this biological vector in rapidly transporting these fallout radionuclides to depth in the Ligurian Sea. In conjunction with sediment trap experiments for directly measuring POC fluxes at the DYFAMED site, several researchers have used an indirect radiometric method to estimate POC fluxes by measuring the disequilibrium between particle reactive short-lived natural radionuclides and their parents (e.g. 234Th/238U and 210Po/210Pb) in the water column, and multiplying the obtained flux (e.g. for 234Th) with the POC/234Th ratio on settling particles. Early studies in the Ligurian Sea had already detected a strong link between 234 Th fluxes and sediment trap recordings [BUA 88] as well as zooplankton biomass and its species composition [SCH 92]. Time-series measurements at the DYFAMED site investigated the seasonal and short-term variability of

Dynamics and Export of POC

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234

Th fluxes [SCH 02], and, during studies carried out within the MedFlux program, large volume in situ pumps were deployed for the simultaneous sampling of the dissolved and particulate fraction of radionuclides in order to estimate POC fluxes from obtained measurements [STE 07]. Far fewer studies have used the disequilibrium between 210Po and its parent 210Pb despite strong evidence that 210Po is more closely linked to carbon cycling within the planktonic food chain than 234Th [STE 05]. 2.2. POC in the Ligurian Sea 2.2.1. Carbon biogeochemistry The carbon reservoir of the world ocean (38,000 Pg) is about 50 times higher than that of the atmosphere (762 Pg) and represents approximately 85% of the global carbon pool [SAR 06]. Autotrophic organisms in the upper sunlit layer of the ocean, the euphotic zone, photosynthetically assimilate dissolved inorganic carbon and transform it into particulate organic carbon (POC). While most of this carbon is recycled back into inorganic carbon within the epipelagic ecosystem, the remaining POC is exported to intermediate and abyssal depths by either gravitational flux, through vertical migration of certain marine organisms, or physically by water mass movements. The mechanism by which atmospheric carbon is transformed into organic matter by biological processes in the surface ocean and its subsequent transfer and sequestration in the deep ocean is called the “biological carbon pump” [SAR 06, VOL 85]. Oceanic Carbon Pumps Due to laws that control the balance of partial pressures of CO2 between the surface ocean and the atmosphere, any gradient in CO2 concentration at the interface of these two reservoirs naturally tends to fade. Thus, the increase in the partial pressure of CO2 in the atmosphere recorded since the beginning of the industrial era (1870) would have been even greater if the oceans had not, at the same time, stored nearly 30% of the CO2 resulting from anthropogenic activity (burning fossil fuels, deforestation...). While partial pressures of CO2 in air and water remain of the same order of magnitude because they tend to balance each other, the oceans contain about 50 times more carbon than the atmosphere. This difference is mainly due to the fact that gaseous CO2 in the ocean

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reacts rapidly with water to form carbonic acid, which itself is in equilibrium with bicarbonate and carbonate ions. All these chemical species constitute the carbonate system which represents the dissolved inorganic carbon (DIC) (see Volume 1, Chapter 4 of this book series). The resulting continuous deficit of CO2 in the ocean leads to an influx of atmospheric CO2. All the phenomena that sustain the carbon cycle, which began to be studied half a century ago, are extremely difficult to decipher. One of the reasons for this complexity is that ocean carbon exists in many forms: inorganic and organic, living and detritic, dissolved and particulate, labile and refractory. All these forms are diversified in their composition, are exchanged through a multitude of physical, chemical and biological processes that operate simultaneously and at different time scales, and are constrained by the vertical gradients of the physico-chemical properties of the water column as well as the temporal variability (diurnal, seasonal, annual, pluri-decadal, geological) of the ocean environment. Among the essential components of the ocean carbon cycle are the carbon pumps. This term refers to all the processes that contribute to atmospheric carbon storage by the oceans. The term sequestration refers to the prolonged storage of carbon in the ocean, without exchange with the atmosphere. Its effectiveness can be defined by the time during which carbon remains isolated from the ocean surface. Indeed, if the water bodies carried by general circulation can transport carbon removed from the atmosphere to depth, they also release it tens, hundreds or thousands of years later when they come back into contact with the atmosphere. Therefore, sequestration is only considered definitive and irreversible when carbon is sequestered in sediments in the very long term (millions of years). In practice, only a small fraction of the carbon accumulated within the surface reaches this stage. Examples for such sequestration are the fossilization of organic carbon, which provides oil and gas deposits under the ocean floor, or the mineralization of inorganic carbon, which supplies calcareous sediments and rocks. However, most of the carbon absorbed by surface waters remains in the water column, mainly in the form of DIC, the predominant species of which is bicarbonate. Since the beginning of the industrial era, the ocean has generally behaved as a carbon sink because the net flow of this element from the atmosphere to the ocean is positive, although locally some ocean areas are considered sources because they emit more CO2 into the atmosphere than they absorb. The respective contributions of the source and sink terms determine the distribution of carbon between the atmosphere and the ocean and are therefore essential elements of climate regulation. The multitude of phenomena that contribute to carbon sequestration is ensured by two clearly identified types of pumps, each carrying a distinct form of ocean carbon. DIC and dissolved organic carbon (DOC) are entrained to depth by the physical (or

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dissolution) pump, while the particulate organic carbon (POM) formed within the surface from the DIC is entrained downwards by the biological pumps. These two mechanisms are responsible to varying degrees – about 90% for the biological pump and 10% for the physical pump – for the DIC gradient commonly recorded between the surface and the ocean floor. The physical pump is mainly active at high latitudes where low temperatures increase not only the solubilization of atmospheric CO2 in seawater, but also the density of the latter. These two phenomena contribute to isolate the DIC-enriched water bodies from the surface water and send them to the deep ocean for long times. It is the dissolution of atmospheric CO2 in surface waters and their mixing with subsurface waters that gives high latitudes the property of being important carbon sinks. The biological pumps export part of the inorganic carbon fixed at the surface by phytoplankton to the bottom. Photosynthesis is therefore the first mechanism of the biological pumps, by transforming the DIC of surface waters into POC. This is a very effective mechanism, given that phytoplankton represent only a very small fraction of ocean organic carbon. This stresses the difference between mass and rate; for example, the heart has a small mass, but it moves blood through the whole body. Carbon fixed by phytoplankton into organic matter will fuel all the organisms in the food web and is sequestered through the supply of this organic matter to heterotrophic organisms of mesopelagic and bathypelagic communities. The biological pumps include the following mechanisms. The carbonate pump results from the dissolution of calcium carbonate in the particles that sink. These particles are phytoplankton (e.g. coccolithophorids) or zooplankton (e.g. pteropods) capable of building external skeleton made of particulate inorganic carbon (PIC). The biological gravitational pump (BGP). Denser than water, the actors in the food web will all tend to sediment. The second main mechanism of the biological pump is therefore gravitational settling; the BGP concerns all living and detrital particles: phytoplankton, zooplankton, fecal material and detritus produced by grazing, bacteria, viruses, marine snow. It is generally accepted that the carbon sequestration provided by the gravitational pump is all the more effective when the particles sediment quickly and deeply, so that the degradation of detritus and their remineralization by bacteria to dissolved CO2 is minimized. In fact, only a very small fraction of the carbon from primary production is effectively sequestered in sediments for geological time, the remainder contributing to the vertical gradient of DIC. This progressive degradation of particles during their sinking is reflected in the decrease in their concentration with depth (Martin curve, [MAR 87]). Of course, all processes that promote or alter the

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gravitational settling of particles have been the subject of intense research. Among the most important are the processes of aggregation, ballasting, compaction (fecal pellets), physical, chemical and biological disintegration. The particle injection pumps (PIP). In recent years, it has become apparent that additional export paths need to be identified and added to the gravitational pump in order to balance the carbon cycle budgets predicted by the models (despite their uncertainties). These pathways, grouped under the term Particle Injection Pumps [BOY 19], can export quantities of carbon comparable to those transported by BGP, and, unlike BGP, concern particles that do not sink and DOC. The transport of this carbon at depth is ensured by physical and biological processes. Physical processes, depending on their intensity — mixed-layer pump or large-scale subduction pump — generate a carbon export to depths between 150 m and 1,000 m, i.e. mostly below the permanent pycnocline. Biological processes are linked to vertical migration. The mesopelagic migrant pump is provided by organisms capable of performing nycthemeral migration through the mesopelagic layer: the carbon assimilated at subsurface is released a few hours later at depth (400 m) via mortality, respiration and the production of fecal pellets. This “one-way shuttle” allows the particulate carbon to reach significant depths without being mineralized. Finally, it should be noted that certain species of copepods in high latitudes are at the origin of the so-called seasonal lipid pump. They spend each winter in a state of diapause (hibernation) at depth (between 600 m and 1,400 m) and dissipate the carbon reserves (lipids) that they have previously accumulated on the surface. The fate of dissolved organic matter (DOM) from primary production and from the degradation of POM is currently a major field of study, particularly because of the difficulties of chemical analysis of its various labile, semi-labile and refractory forms, but also because, being carried into the interior ocean by subduction processes, DOM is one of the vectors by which atmospheric carbon fixed at the sea surface can be stored in a sustainable manner. Similarly, we must mention the relatively recent discovery of the microbial carbon pump, which accelerates the transformation of labile C into refractory C which, difficult to remineralize, can remain in this form for millennia in the deep ocean (see Volume 1, Chapter 7 of this book series). The respective contributions of these different biological pumps are difficult to establish for three reasons: (1) they interfere with each other; (2) because of the physical processes involved, understanding how they work requires 4D observation and modeling approaches, unlike the BGP, which a 1D study can constrain as a first approximation; (3) their characteristic operating scales are very different and spatiotemporally variable. Among all that remains to be discovered, the processes that modify particles between the time they are exported to depth and the time they reach the permanent pycnocline are still very poorly understood. We can now rely on recent

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developments in imaging and acoustics on autonomous floats to better discern, within a 4D system, the nature of particles (zooplankton vs. detritic) and their interaction, via their size distribution, which is an essential but currently missing element in biogeochemical models of the ocean. These modeling issues for climate prediction are crucial at a time when there are serious questions about the ability of the oceans to continue to function as a carbon sink, as they have done since the beginning of the industrial era. There are indications that this is no longer entirely the case. One example is ocean acidification, which reflects an increase in CO2 content resulting from the saturation of the buffer capacity of the carbonate system. The positive or negative feedbacks of climate change on the ocean (pCO2, temperature, stratification, circulation...) and on the ocean carbon pump (and vice versa) are extremely difficult to anticipate, as evidenced by the variability of predictions from coupled physical/biogeochemical models. Heating surface water can have direct effects on the carbon pump, for example by reducing the solubilization of atmospheric CO2 in the ocean. But the effects can also be antagonistic on the export of material. Warming can, on the one hand, stimulate the primary production of poikilothermic phytoplankton organisms, but, on the other hand, promote the emergence of more adapted species, but of smaller sizes and, therefore, less conducive to sedimentation. The intensification of stratification and the prolongation of its annual occurrence will, according to modeled projections, be likely to limit primary production by reducing the upwelling of nutrients in oligotrophic areas (in the Mediterranean, this is referred to as “tropicalization”), but could stimulate it at high latitudes due to the melting of the ice caps. The increased stratification is also a physical barrier to the export of carbon to the bottom.

The biogeochemistry of particulate carbon in the Ligurian Sea is substantially influenced by the seasonal cycle of biological production, which depends on physical conditions of mixing and stratification of the water column (see Volume 1, Chapter 6 of this book series). During the winter mixed period, nutrients are injected into the photic zone and enable the blooming of phytoplankton in spring, when atmospheric warming of the surface waters leads to the stratification of the water column. Throughout the summer and into autumn, the established density gradient, the pycnocline, prevents a further supply of nutrients from deep waters. The only source of nutrients in the photic zone is provided by the regeneration of organic matter, which reduces significantly biological production during these seasons. Such seasonality is generally observed in the temperate zone at mid-latitudes where seasonal and also interannual variabilities are among the highest.

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The production of POC in the Ligurian Sea directly depends on those variabilities, which have been studied extensively with respect to phytoplankton production [MAR 02a], zooplankton community changes [MOL 08], particle dynamics [STE 02] and POC export [MIQ 11]. As primary production over the whole Mediterranean Sea is rather low, it is considered as being oligotrophic [MAR 85, MIN 88, SOU 73]. However, there are important regional differences and the Ligurian Sea is one of the most productive regions [BOS 04, DOR 09]. An important driver of this productivity is the winter mixing, which is more pronounced in the northwestern part of the Mediterranean than in most other areas. Early studies have already shown that the Gulf of Lion is an area of deep-water formation [MED 70], and more recent field studies in the northwestern Mediterranean demonstrated the consequences of these mixing events on the carbon cycle [MAR 10b, MAY 17a], which have been confirmed by modeling approaches [AUG 14, HER 13]. Depending on their size and/or density, organic particles will either remain suspended or sink down in the water column, which has important implications for the carbon biogeochemistry. As such, suspended particles are related to dissolved organic matter since their fate and behavior depend mainly on hydrodynamics, while sinking particles are also subject to gravitational forces [SAR 06]. This poses a major problem in observing and measuring POC dynamics. Particles can be sampled by filtration or pictured by in situ photography, and their size determined using different mesh sizes and optical measurement tools respectively, but neither method is able to determine whether the particles are sinking or non-sinking. A key issue is therefore to understand the mechanisms that transform non-sinking into sinking particles or vice versa (e.g. aggregation, disaggregation). These mechanisms have been studied extensively in the past by both direct observations and modeling approaches [ALL 95, BUR 09], and have furnished insights into the dynamics of suspended particles and their role in the carbon cycle. Sinking particles, however, can be sampled directly by sediment traps. These particles, mostly organic aggregates, are a key component of the biological pump (Figure 2.2). They are formed from biogenic detrital particulates such as fecal pellets from zooplankton and nekton feeding activities, phytoplankton detritus, crustacean zooplankton molts, carcasses, shed eggs, discarded mucous feeding structures from larvaceans and salps, and amorphous fragile “marine snow” [FOW 86, GOR 84, SIL 91, TUR 15].

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Figure 2.2. Different types of marine organic particles. Fecal pellets are distinguishable from other particles by a clear outline (elliptical, cylindrical (long or short), irregular, etc.). Some carcasses of mollusks and foraminifera are marked with a white arrow. For a color version of this figure, see www.iste.co.uk/migon/ mediterranean2.zip

In the Ligurian Sea, early field studies, sediment trap experiments and laboratory analyses demonstrated the importance of biogenic particulates of planktonic origin, particularly zooplankton fecal pellets, in the export of carbon and other elements from surface waters [CHE 75, FOW 77, FOW 79, FOW 91]. With the following development of advanced, time-series sediment traps using rotating collection cups, it became possible to moor traps for longer periods of time in order to study the evolution of sinking biogenic particulates with respect to specific types over both time and depth [CAR 98, MIQ 11, MIQ 94].

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2.2.2. Export flux, key contributors and processes Within the last 30 years, the reported data on export flux of particulate organic carbon in the Ligurian Sea were almost exclusively obtained at the DYFAMED time-series station (43°25’N, 7°52’E), a site 28 nautical miles off the coast of Villefranche-sur-Mer. However, the first studies within the DYFAMED program were carried out at a station approximately 15 nautical miles off the coast of Calvi, Corsica. They confirmed findings from earlier studies at coastal sites [FOW 91], which showed that fast sinking particles such as fecal pellets produced by zooplankton represent an important vector for transporting carbon down the water column. A fortunate natural field experiment gave striking proof of this transfer efficiency when the particles collected at 200 m depth contained artificial radionuclides from the unfortunate nuclear accident at Chernobyl [FOW 87]. However, these early offshore studies also highlighted the role of physical mixing and seasonality in the temporal variability of vertical particle flux. They also demonstrated the attenuation of flux with depth and seasonal differences in the composition of the sinking particles [MIQ 94]. Similar results were shown in a longer time series, which combined these data with the first data from the permanent DYFAMED time-series station [MIQ 95]. Continuous measurements of vertical flux at this station were necessary in order to understand and better analyze the emerging patterns. Miquel et al. [MIQ 11] presented such an analysis for the data obtained over two decades. This is the longest existing series of flux data in the Mediterranean and also one of the longest worldwide (Figure 2.3). The particle flux presented both as bulk mass and particulate organic carbon (POC) exhibited a huge variability over the reported time period. The range between minimum and maximum fluxes covered more than two orders of magnitude with mass flux values ranging from 1 g m–2 d–1 and POC fluxes from < 1 mg C m–2 d–1 to > 50 mg C m–2 d–1. Within these variabilities, Miquel et al. suggested a shift from a decade with relatively low variabilities to a decade, beginning in the late 1990s, with more frequent appearances of extreme values. Such peaks of flux, even at daily scales, were reported from a study dedicated to short-scale variability at the DYFAMED site [AND 09, MAR 09].

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Figure 2.3. Time series of POC flux recorded in sediment traps at two depths (200 m, 1,000 m) of the DYFAMED station from 1988 to 2005. The bar width represents the sampling period for individual samples ranging from 7 to 15 days. Data gaps in 1992 and 1996 are due to loss of the mooring line (from [MIQ 11])

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Despite significant interannual differences, a clear seasonal flux pattern could be observed. At 200 m depth, maximum export fluxes were observed during the winter and the spring, towards the end of winter for mass flux, and in spring for POC flux. The maximum average fluxes over the observed time period amounted to some 300 mg m–2 d–1 and approximately 20 mg C m–2 d–1 for mass and POC flux respectively, although the variation coefficients of these means were approximately 50%, indicating a high interannual variability [MIQ 11]. Throughout the summer and into the autumn, average mass fluxes remained mostly below 50 mg m–2 d–1 and always below 100 mg m–2 d–1, while POC flux values were approximately 5 mg C m–2 d–1. Still, in early summer, POC flux pulses occasionally observed over the 20-year study period were responsible for the relatively high mean flux values and consequently high standard deviations similar to those of the mean maximum fluxes. These seasonal patterns demonstrated that POC fluxes in the Ligurian Sea are in fact strongly related to the seasonal cycle of mixing and stratification of the water column generally observed in mid-latitude seas. Winter mixing favors not only vertical transport of particulate matter but also primary production through nutrient supply from depth, which in turn yields higher POC fluxes. In contrast, summer stratification hinders not only the nutrient supply from depth but also the transport of particles from surface to depth through the establishment of a density barrier, the pycnocline. In an earlier study on the transfer of atmospheric inputs through the euphotic layer, Migon et al. [MIG 02] proposed a three-step scenario that describes the annual flux pattern (see Volume 1, Chapter 5 of this book series): – during the winter, a physical process, dense water formation, is responsible for the vertical transport of significant amounts of particulate matter containing lithogenic material; – during spring, biological activity determines the strength of vertical flux by the efficiency and ways of transforming suspended organic particles into dense sinking particles; – during summer and autumn, the stratification of the water column generally prevents the vertical transfer of matter, which accumulates along the pycnocline and may lead to wind-driven episodic flux events. According to Miquel et al. [MIQ 11], POC flux seemed to be more consistently related to vertical mixing, expressed by the mixed layer depth,

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than to the observed phytoplankton biomass. From a similar study, Heimbürger et al. [HEI 13] argued that the magnitude of the mixed layer depth determines the magnitude of vertical export flux, in a direct way during winter and indirectly during spring, by the magnitude of nutrient supply for biological production. The seasonality at 200 m depth was also observed at 1,000 m depth over the two-decade study period reported by Miquel et al. [MIQ 11]. Maximum average fluxes occurred towards the end of the winter and in late spring – early summer, the reported values being approximately 200 mg m–2 d–1 for mass flux and almost 10 mg C m–2 d–1 for POC. The minima, which were recorded during the late summer and autumn months, were similar for mass flux (50 m d–1 between these two depths. Over the whole study period, Miquel et al. reported a transfer efficiency from 200 m to 1,000 m, close to 90% for the mass transfer and 60% for the transfer of POC. The similar seasonality and the relatively efficient transfer of particles between the two depths suggest, again, that seasonal vertical mixing is one of the main driving forces of particle flux in this area, which impacts most, if not all, of the water column [HER 13]. Ever since the seminal publications distinguishing between new and regenerated production [DUG 67] and introducing the f ratio [EPP 79] between new and total production, and the definition of the e ratio (export/primary production) by Downs [DOW 89], these ratios have become of primary interest in studies on the strength of the biological pump in the oceanic carbon cycle. As Eppley and Peterson [EPP 79] put it, at appropriate scales of time and space, POC exported from the euphotic layer should be balanced by new production, for the production system not to run down. In the Ligurian Sea, early estimates of the e ratio were published by Miquel et al. [MIQ 94], who reported an average ratio of 5–7% from flux measurements at 200 m depth over a 15-month period. This was in contrast to earlier estimations of 13–39% in the same area, which were based on primary production and nutrient supply measurements [BET 89, MIN 88].

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More recently, even lower e ratios ranging from 0.5% in autumn to 1.7% in winter were obtained at stations located in the western and mostly in the northwestern Mediterranean basin [RAM 16]. These results were based on flux data at 200 m depth, either directly measured by sediment traps or calculated from particle size distribution measurements, while primary production was estimated from satellite data. Another study, carried out at 20 stations, distributed over the entire Mediterranean Sea, in early summer, used drifting sediment traps at 200 m depth deployed during 8 h and 24 h. The e ratio from the northwestern Mediterranean station was estimated to be 12.5% [MOU 02], with an average of 4% for the whole study area. A value of just over 11% was calculated from flux recordings of sediment traps deployed at 100 m depth at the outer margin of the Gulf of Lion in the northwestern Mediterranean [GOG 14]. The great variability of e ratios, spanning over more than one order of magnitude, reported in these studies, was related to seasonal and geographical differences and, perhaps more importantly, to methods used in measuring and/or calculating the POC flux and the depth-integrated primary production. The base of the euphotic zone (1% light level) is a commonly used depth for comparing these two measurements [BUE 98]. However, in practice, such a standard depth and method may be achievable during a particular study, but hardly ever over more extended spatial and temporal scales. Still, the data obtained in the Ligurian Sea from the DYFAMED time series indicate some trends about the export efficiency. Over the study period, 1988–2005, annual POC fluxes at 200 m remained relatively stable [MIQ 11], but in the first decade of the period, there was an increasing trend in phytoplankton biomass [MAR 02b], which indicates a decreasing trend in export efficiency. This shift towards a more regenerated production regime was also represented by a change in the phytoplankton community composition from micro- to pico- and nanophytoplankton [MAR 02a, MAR 02b]. However, for the second decade, Marty and Chiaverini [MAR 10b] observed a shift towards an increase in export efficiency, due to the more frequent appearance of intense phytoplankton blooms dominated by microphytoplankton, especially diatoms. This shift corresponded to the shift in flux regime, from one with relatively low amplitudes in flux variability, to one with frequent extreme flux pulses [MIQ 11]. The removal of POC from the ocean surface expressed by the e ratio indicates the strength of the biological carbon pump. Its efficiency can be measured by comparing the export flux to the flux at 1,000 m depth or below, where carbon is considered to be stored for centuries or millennia

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[PAS 12], and which is normally not reached by mixing of the surface waters (e.g. seasonal mixing at mid-latitudes) over these relevant time scales for carbon sequestration [LAM 08]. This depth is also the lower limit of what is commonly known as the twilight zone. The northwestern Mediterranean Sea is a well-known site of deep-water formation [CON 18, MED 70], and mixing beyond 1,000 m depth has been observed in the Gulf of Lion [MAY 17b] and the Ligurian Sea [MAR 10b]. Nevertheless, Miquel et al. [MIQ 11] showed, in their two-decade study, that winter mixing did not reach that depth. They also compared fluxes registered at 200 m and 1,000 m and observed an average annual POC transfer efficiency of 60%, which was highest during the summer period (>80%) and lowest (approximately 50%) during autumn and winter. This is considerably higher than the 10% measured in a one-year study in the Gulf of Lion [GOG 14], although these fluxes were measured at 100 m and 1,200 m depth. Even taking into account a flux attenuation of 60% between 100 m and 200 m [GUY 15], the transfer efficiency would still be less than half of the one from the two-decade study. Similar estimates of some 10–20% were obtained in more global studies of the POC transfer efficiency through the mesopelagic layer [AUM 17, HEN 12]. These authors also showed that in areas of high export flux, the transfer efficiency is rather low, while in areas of low export flux it is rather high. In the Ligurian Sea, and on a seasonal scale, a relatively high transfer efficiency was observed in spring and summer as POC flux declined from its maximum to its minimum values, and a relatively low efficiency, starting from this minimum and lasting until the end of winter, when the flux was again at its highest [MIQ 11]. A study aiming at understanding the processes that govern flux attenuation across the mesopelagic layer was carried out at the DYFAMED site between 2003 and 2007 [LEE 09a]. The study, called MedFlux, was motivated by the ballast ratio hypothesis [ARM 02], which is based on the observation that below a certain depth (>1,800 m), POC and the associated mineral ballast (carbonates, opal, dust) fluxes are observed at a nearly constant ratio. In order to get more insight into the mechanistic aspects of this association, new techniques for sampling settling particles were used. They enabled the authors not only to collect sufficient material for analyzing its chemical composition, but also to obtain particles according to their settling velocity [PET 05]. Lee et al. [LEE 09b] showed that ballast material of both planktonic and atmospheric origin enhances particle flux, by serving as a “nucleator” for particle aggregation within the photic layer. However, they observed hardly any effect of ballast material on the particle sinking

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velocity, and atmospheric dust input was related to mass flux but not to surface productivity. This latter finding was confirmed in an analysis of a two-decade time series of export fluxes at the DYFAMED site [HEI 13]. Another major finding of the MedFlux study came from the settling velocity measurements. Particles settling at well over 200 m per day constituted the major part (>60%) of mass flux [ARM 09] and about 25% of POC flux [SZL 09]. Many of the POC flux data obtained during the MedFlux study were estimated by using radionuclides from the naturally occurring uranium-238 decay series. Short-lived radionuclides of the U/Th series and in particular 234 Th and 210Po have been used since the 1990s to study POC fluxes (e.g. [BUE 92, MUR 05], for a review see [COC 03]). Both these radionuclides are scavenged by settling particles, while the parent radionuclides (238U, 210Pb) show a more conservative behavior, 238U remaining in solution and 210Pb adsorbing to particles but not being accumulated in organic tissues, as is the case for its granddaughter 210Po [HEY 76, STE 03]. This leads to a disequilibrium between these pairs of radionuclides in the upper ocean, due to the export of sinking particles. The deficit of the scavenged radionuclide integrated over a given depth range, multiplied by the POC/234Th or POC/210Po ratio of the settling particles, corresponds to the POC flux out of that depth range. 238U concentrations are generally derived from salinity due to their linear relationship [CHE 86, OWE 11]. Deviations from this relationship, especially for the Mediterranean Sea, have been observed [SCH 91], but they were thought to be systematically biased [DEL 02, PAT 07]. During the MedFlux study, the concurrent measurements of vertical particle flux by sediment traps and by using radionuclides as tracers highlighted some fundamental aspects of particle dynamics. While the deficit of radionuclides is only driven by settling particles, the dissolved phase of these radionuclides is subject to water mass movements, as are suspended particles. Radionuclide-derived estimations of POC flux are therefore not necessarily comparable to sediment trap measurements, which record the flux of only settling particles. In a rapidly changing environment (wind-induced mixing, spring phytoplankton blooms, etc.), the spatial scales upon which these two approaches depend are significantly different [COC 09]. Environmental conditions will also influence, for example, the

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scavenging process of radionuclides, due to aggregation and disaggregation dynamics [ABR 10, SZL 09] or the steady-state, non-steady-state assumption of the radionuclide deficits for the estimation of POC flux [STE 07]. The methodological advancements achieved during MedFlux allowed the gaining of more insight into rather mechanistic aspects of particle dynamics and flux, whereas studies during the preceding decade were investigating rather biological aspects of the origin and fate of sinking particles. In particular, zooplankton fecal pellets were consistently a prominent component of the sediment trap samples. In a study carried out off Calvi, Corsica, from January 1987 to June 1988, they were enumerated according to the different shape classes present [MIQ 94]. The total numerical pellet flux through 200 m during the first months of the year averaged 3.74 × 104 pellets m–2 day–1, and was higher than during August, with 1.6 × 103 pellets m–2 day–1, which may, among other factors, reflect higher pellet recycling activity via coprophagy and bacterial degradation. The principal forms found were cylindrical pellets from large copepods and euphausiids [FOW 72], elliptical shapes produced by smaller copepods and amphipods [SAS 81], and very small spherical pellets, likely released by tiny invertebrates and protozoans [HEI 88] (Figure 2.4). Intact salp pellets (“flakes”) were fairly rare in the traps, although they are often abundant at certain times of the year, particularly during spring. This suggests that, despite their very high sinking speeds, for example 400–2,700 m day–1 [FOW 86], they are most likely consumed and broken down during transit through the water column. The relative distribution of the different forms varied greatly between the seasons. In January–May, elliptical (44%) and spherical (54%) forms comprised virtually all of the sedimenting pellet population, while in summer, cylindrical forms comprised 40% of the pellets and elliptical and spherical pellets approximately 30% each. The most striking observation was a directly proportional correlation between the numerical fecal pellet flux and the total particulate carbon flux through the water column. Furthermore, when numerical pellet flux was converted to carbon flux, the contribution of pellet carbon flux to total carbon flux ranged from approximately 2% to 62%, with the maximum occurring in February.

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Figure 2.4. Different types of fecal pellets and the corresponding planktonic organisms that produce them (Salps, credit: D. Luquet; Pteropods, credit: C. Sardet (plankton chronicles); Euphausiids, credit: Ø. Paulsen (mar-eco.no); Copepods, credit: S. Gasparini (copepods of Villefranche Bay)). The sizes of each type of pellets may vary considerably and according to the size of the individual organisms and the species within the plankton groups. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

The presence of algal aggregates among the sinking particulates was detected by the specific organic biomarker composition of the trap samples, for example, the C17 n-alkanes, which are a typical component of phytoplankton but are not found in zooplankton fecal pellets [MAR 94]. Analyses indicated that in the period of maximum biological activity (March–July), phytoplankton detrital inputs were highest in April, with the highest zooplankton biogenic particulate inputs following in late June and July. In a follow-up, more detailed study, Carroll et al. [CAR 98] analyzed zooplankton fecal pellets in trap samples from four depths (200 m, 500 m, 1,000 m and 2,000 m) on a mooring at the DYFAMED site during 1990. The pellet fluxes were numerically and seasonally roughly similar to those measured earlier at 200 m in open waters off Corsica [MIQ 94]. The only

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two spring months, April and May, represented 50% of the integrated annual fecal pellet flux and 62% of pellet carbon. Interestingly, the maximum numerical fluxes were noted at 1,000 m depth, suggesting some fecal pellet production below the euphotic zone. Nevertheless, there appeared to be a lower pellet carbon content with depth, indicating bacterial degradation or possible repackaging through grazing of the sinking pellets. The different pellet types and shapes were similar to those mentioned above, and elliptical pellets together with spherical pellets accounted for 88% of the numerical pellet flux. Although being relatively low in abundance, the large size of the cylindrical pellets relative to the other types resulted in their large average contribution (39%) to the overall pellet carbon flux. An important contribution of this pellet type, observed only at 500 m, was due to the influence of the abundance of a large subtype of elliptical pellet, >350 µm or roughly three times the length of the dominant smaller elliptical type. Again, large salp flakes were not a significant contributor to the numerical or pellet carbon fluxes, but a later assessment of similar data covering 17 years from 1988 to 2005 indicated an increase in large salp fecal pellets in trap samples from 1999 onwards at the DYFAMED station [MIQ 11]. Because the central Ligurian Sea does not present any particular hydrographic feature or anomaly, Carroll et al. [CAR 98] suggested that there may be a resident mid-water zooplankton or nekton community that repackages sinking particulates at that depth and forms these large cylindrical pellets. This possibility needs to be investigated in future studies. The relative contribution of pellet carbon to the total particulate carbon flux at the DYFAMED station varies both temporally and with depth. In 1990, the proportion of total particulate carbon in fecal pellets generally decreased in significance with depth varying, on average, from 24% at 200 m to 8% at 2,000 m. The integrated water column particulate carbon flux averaged over all depths was estimated to be approximately 5.7 mg C m−2 day−1. Of that total particulate flux, only 18% (approximately 1 mg C m−2 day−1) is transported via fecal pellets. Nevertheless, the contribution of pellet carbon to the total particulate flux was not consistent throughout the year; it varied from 35% in January when the water column is well mixed to only 3% in September under stratified water column conditions. Besides fecal pellets, DYFAMED field studies using sediment traps have identified other biogenic debris in the trap samples, for example, crustacean

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molts, eggs, zooplankton carcasses, protozoa and algal cells, both intact and fragmented, and amorphous flocs or marine snow particles of undetermined origin. However, because of the transient and sporadic nature of such materials and the difficulty in adequately quantifying them, little effort has gone into comparing their carbon contribution to the total carbon flux in northwestern Mediterranean samples. Difficulties arise because the composition of amorphous flocs and particles changes drastically over time. For example, during periods of low flux, material in traps was a mixture of greenish fluffy aggregates containing zooplankton fecal pellets of high carbon content, whereas during episodes of high flux the material often had a more compacted, muddy appearance, reflecting a strong input of clay mineral particles, probably due to terrigenous inputs [MIQ 11]. Furthermore, with respect to flocs, at times, during periods of prolonged stratification in the water column, traps have become completely clogged with large amounts of mucilaginous matter, as occurred in 2002, which precluded separating other biogenic particles within it [MAR 10a]. Thus, although intact fecal material is easily identified and sampled, the other mixed components of the mass flux are very difficult to separate as well as to determine the origin of. 2.2.3. Modeling POC dynamics Deciphering the complete composition of organic particles in flux samples from a sediment trap is a tedious and, in some cases, impossible task. As the deployment of traps became a regular scientific activity in the Ligurian Sea, an early answer of scientists to this problem was the development of models to gain more insight into the origin and nature of the biogenic particles. The export of particulate organic matter became an integral part of such models, which simulated the functioning of the pelagic ecosystem. In a first approach, living and dead phytoplankton and two herbivore plankton groups, copepods and salps and their fecal pellets, were considered. The model outputs showed that fecal pellets represented 33 mg C m−2 d−1 of a total of 45 mg C m−2 d−1 of the vertical particle flux over a simulated 40-day period. In particular, salp carcasses and fecal pellets made up 72% of the total flux [AND 88]. After this model, based on coastal conditions, a coupled physical-biological model was elaborated to study an annual cycle, expressed in terms of nitrogen, of the stocks and fluxes in and across different ecosystem compartments (phytoplankton, zooplankton, bacteria, dissolved and particulate organic matter, etc.). The model paid particular attention to the fluxes of particulate and dissolved matter exported

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from the surface layer. Simulations were carried out for the offshore DYFAMED time-series station, the dataset of which was used to validate the simulation runs [LEV 98]. The model estimated the 1991 annual POC flux at 3.9 g C m−2 y−1, compared to the mean value of 4 g C m−2 y−1 measured for the 1987–1990 period [MIQ 94], although it was not able to reproduce flux peaks during the winter. Among other results from the model runs were vertical fluxes of small and slowly sinking particles and of diffusive fluxes of detritus, bacteria and phytoplankton. Finally, it demonstrated that the export of refractory organic matter during the winter mixing period could exceed the POC flux threefold. With the observational datasets, especially from the DYFAMED time-series station, covering decades, questions about trends and prospections of the ecosystem functioning in future climate change scenarios started to arise, which models should be able to answer. One such model is the three-dimensional coupled physical-biogeochemical model that explored the possible changes in the ecosystem of the northwestern Mediterranean under present (at the end of the 20th Century) and future (at the end of the 21st Century) climate conditions [HER 14]. Initiated by data obtained from the DYFAMED time series, the model simulations showed that the main changes under the future climate scenario are related to the weakening of the deep convection of the water column during the winter due to surface warming. This induces a significant increase of the dissolved organic carbon concentration in the top 200 m layer, but it changes neither the total particulate carbon concentration nor the POC export. Another model focused not on the temporal but on the spatial scale, in order to extend the observational data restricted to one or a few measurement stations to the entire Mediterranean basin [GUY 15]. The three-dimensional model combined a high-resolution hydrodynamic model with a mechanistic biogeochemical model to investigate organic carbon export fluxes. The results of the model run revealed a clear increasing gradient in POC export flux from east to west, contrasting with a rather even distribution over the whole Mediterranean basin of dissolved organic carbon (DOC) fluxes. These latter fluxes were responsible for roughly 80% of the total organic carbon fluxes. According to the model outcomes, an increase in DOC production could be expected, due to enhanced water column stratification, as was the case in the simulations of the model reported by Herrmann et al. [HER 14]. Alternatively to the development of models on the vertical POC flux, new methods were explored for observing the particulate matter in situ. In the

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Ligurian Sea, the first data from photographic recordings of suspended aggregates were reported almost 30 years ago [GOR 92]. This in situ imaging technique was further developed, and the most recent version of the instrument, the Underwater Vision Profiler (UVP), can be coupled with a CTD and integrated into a CTD-rosette sampler [PIC 10]. Optical particle size measurements can be done at very high frequencies and very accurately, although generally limited to particles >100 µm in diameter. This has the advantage of building on statistical values and allowing a mechanistic approach in studying particle dynamics. In the Ligurian Sea, it has been used as a major tool for studying particle dynamics at highly resolved spatial and temporal scales [GOR 00, STE 02]. The results of substantial amounts of particle size measurements could be transformed into particle size spectra, and the patterns obtained were analyzed by using models on the different bio-physical mechanisms of particle transformation (aggregation, fragmentation, consumption, remineralization, etc.). It showed the importance of mesozooplankton grazing in the removal of large sinking particles and, at depth, of bacterial activity in the remineralization of smaller particles [STE 04]. Particle size spectra of large sinking particles were used to calculate instantaneous particle flux by integrating mass and settling rate of a given particle size over the entire size spectrum [GUI 08]. In an extensive study covering the whole Mediterranean Sea, Ramondec et al. [RAM 16] demonstrated that POC flux estimates calculated from the results obtained by the UVP particle size measurements compared well to the fluxes recorded by drifting moorings of sediment traps. Specifically, the data from the DYFAMED study site showed that this relationship could be observed on a short temporal as well as a broad spatial scale. 2.3. Present status of POC flux and dynamics in the Ligurian Sea Scientists studying zooplankton and their chemical composition soon realized that a number of trace elements and radionuclides showed exceptionally high concentrations in their shed exoskeletons and fecal pellets. Fecal pellets especially, being produced at relatively high rates (2,000 m). The DYFAMED (Dynamics of Atmospheric Fluxes in the Mediterranean) program and its time-series station was and still is an integral part of scientific studies focusing on global biogeochemical cycles. Over 30 years of field work and measurements in the Ligurian Sea have contributed to a number of important findings (see also elsewhere in this volume). The results on POC flux have highlighted the importance of long-term studies. They were necessary to reveal seasonal and interannual variabilities, which could be related respectively to the yearly hydrological cycle of mixing and stratification of the water column, and to nutrient inputs and the community composition of primary producers. The POC flux data have also provided clear evidence for the rapid transfer of atmospheric inputs from the surface to the deep ocean, mediated mainly by zooplankton activity. The ballast hypothesis, i.e. the deterministic role of minerals in the vertical POC flux, has been described in more detail, by showing that minerals are deterministic in the nucleation of sinking particles, rather than in the transfer at depth of particulate organic matter. The Ligurian Sea and especially the DYFAMED time-series site also served as a platform for the development and testing of new sampling and observation methods. The spatial and temporal, resolution of data from sediment traps being quite low, measurements using natural radionuclides as tracers for POC flux were used to get more frequent flux profiles during periods of rapid transition of the physical environment. Instruments with modern imaging techniques and real-time image analysis were deployed and provided results on the distribution and flux of particulate matter with high spatial, as well as high temporal, resolution. Finally, these datasets could be used to develop and validate new basin-scale models of vertical POC flux for the whole Mediterranean Sea.

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In the era of global change, the carbon cycle is of utmost importance, as is the ocean’s capacity to absorb and store atmospheric carbon dioxide. A key driver in this process is the biological carbon pump. Its precise understanding conditions our ability to forecast future changes and to provide a scientific basis for actions to mitigate the negative impacts of global change. Research on POC flux in the Ligurian Sea is now extending its sampling strategy to the entire northwestern Mediterranean basin within the activities of the MOOSE program [COP 19]. It continues the long-term measurements and monitors POC flux at several mooring sites, which are completed by recordings of particulate matter by autonomous vehicles. Tracking the carbon with these modern sampling methods should be accompanied by field and laboratory studies of the biological factors that govern the fate of oceanic carbon, in order to complete the picture of the biological carbon pump. The traditional notion of particles itself should be completed by extending it to transparent exopolymer particles (TEP) when continuing past studies oriented at providing a mechanistic understanding of oceanic carbon flux. TEP play an important role in the cycling of organic carbon in the euphotic zone and are likely to impact the remineralization process [MAR 17]. The remineralization of particulate organic matter has been recognized since the very beginning of POC flux investigations. It has been observed that the attenuation of carbon flux with depth, in part due to remineralization, follows a power function that led to the hypothesis that such an empirical relationship, an asymptotic curve – the so-called “Martin Curve” – could be used to predict carbon flux at any given depth in the northeast Pacific [MAR 87]. Since global biogeochemistry models have shown that atmospheric carbon dioxide concentrations are highly sensitive to the depth at which oceanic, particulate organic carbon is remineralized back to carbon dioxide [KWO 09], this process has drawn considerable attention among scientists and should also be considered in future POC flux research. Finally, the importance of maintaining time-series studies cannot be sufficiently emphasized. Henson et al. [HEN 16] showed that, in order to distinguish a climate change-driven trend in POC export from natural variability, roughly 30 years of data are necessary. The dataset from the Ligurian Sea on POC export represents one of the longest existing time series, from which we have learned that the Mediterranean Sea is probably more sensitive to climate change than other oceanic regions. Its predictive potential may elevate it to a key reference area in future global biogeochemistry research.

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[MIQ 95] MIQUEL J.C., FOWLER S.W., MOSTAJIR B. et al., “Long term study of particulate carbon flux in the open NW Mediterranean Sea”, Global Fluxes of Carbon and its Related Substances in the Coastal Sea-Ocean-Atmosphere System. M&J International, Yokohama, Japan, 1995. [MIQ 11] MIQUEL J.-C., MARTÍN J., GASSER B. et al., “Dynamics of particle flux and carbon export in the Northwestern Mediterranean Sea: A two decade time-series study at the DYFAMED site”, Progress in Oceanography, vol. 91, pp. 461–481, 2011. [MOL 08] MOLINERO J.C., IBANEZ F., SOUISSI S. et al., “Climate control on the long-term anomalous changes of zooplankton communities in the northwestern Mediterranean”, Global Change Biology, vol. 14, pp. 11–26, 2008. [MOU 02] MOUTIN T., RAIMBAULT P., “Primary production, carbon export and nutrients availability in Western and Eastern Mediterranean Sea in early summer 1996 (MINOS cruise)”, Journal of Marine Systems, vol. 33, pp. 273–288, 2002. [MUR 05] MURRAY J.W., PAUL B., DUNNE J.P. et al., “Th-234, Pb-210, Po-210 and stable Pb in the central equatorial Pacific: Tracers for particle cycling”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 52, pp. 2109–2139, 2005. [OWE 11] OWENS S.A., BUESSELER K.O., SIMS K.W.W., “Re-evaluating the 238Usalinity relationship in seawater: Implications for the 238U–234Th disequilibrium method”, Marine Chemistry, vol. 127, pp. 31–39, 2011. [PAS 12] PASSOW U., CARLSON C.A., “The biological pump in a high CO2 world”, Marine Ecology Progress Series, vol. 470, pp. 249–271, 2012. [PAT 07] PATES J.M., MUIR G.K.P., “U-salinity relationships in the Mediterranean: Implications for Th-234:U-238 particle flux studies”, Marine Chemistry, vol. 106, pp. 530–545, 2007. [PET 05] PETERSON M.L., WAKEHAM S.G., LEE C. et al., “Novel techniques for collection of sinking particles in the ocean and determining their settling rates”, Limnology and Oceanography – Methods, vol. 3, pp. 520–532, 2005. [PIC 10] PICHERAL M., GUIDI L., STEMMANN L. et al., “The Underwater Vision Profiler 5: An advanced instrument for high spatial resolution studies of particle size spectra and zooplankton”, Limnology and Oceanography – Methods, vol. 8, pp. 462–473, 2010. [RAM 16] RAMONDENC S., GOUTX M., LOMBARD F. et al., “An initial carbon export assessment in the Mediterranean Sea based on drifting sediment traps and the underwater vision profiler data sets”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 117, pp. 107–119, 2016.

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[SAR 06] SARMIENTO J., GRUBER N., “Carbon cycle, CO2, and climate”, Ocean Biogeochemical Dynamics, Princeton University Press, 2006. [SAS 81] SASAKI H., NISHIZAWA S., “Vertical flux profiles of particulate material in the sea off Sanriku”, Marine Ecology Progress Series, vol. 6, pp. 191–201, 1981. [SCH 91] SCHMIDT S., REYSS J.L., “Uranium concentrations of Mediterranean seawaters with high salinities”, Comptes Rendus de l’Academie des Sciences Serie II, vol. 312, pp. 479–484, 1991. [SCH 92] SCHMIDT S., REYSS J.L., BUAT-MENARD P. et al., “Relation between 234Th scavenging and zooplankton biomass in Mediterranean surface waters”, Oceanologica Acta, vol. 15, pp. 227–231, 1992. [SCH 02] SCHMIDT S., ANDERSEN V., BELVISO S. et al., “Strong seasonality in particle dynamics of North-western Mediterranean surface waters as revealed by 234Th/238U”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 49, pp. 1507–1518, 2002. [SIL 91] SILVER M.W., GOWING M.M., “The particle-flux: Origins and biological components”, Progress in Oceanography, vol. 26, pp. 75–113, 1991. [SMA 79] SMALL L.F., FOWLER S.W., UNLU M.Y., “Sinking rates of natural copepod fecal pellets”, Marine Biology, vol. 51, pp. 233–241, 1979. [SOU 73] SOURNIA A., “La production primaire planctonique en Méditerranée. Essai de mise à jour”, Bulletin de l’Étude en Commun de la Méditerranée, vol. 5, pp. 1–128, 1973. [STE 02] STEMMANN L., GORSKY G., MARTY J.-C. et al.,“Four-year study of large-particle vertical distribution (0–1000m) in the NW Mediterranean in relation to hydrology, phytoplankton, and vertical flux”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 49, pp. 2143–2162, 2002. [STE 03] STEWART G.M., FISHER N.S., “Experimental studies on the accumulation of polonium-210 by marine phytoplankton”, Limnology and Oceanography, vol. 48, pp. 1193–1201, 2003. [STE 04] STEMMANN L., JACKSON G.A., GORSKY G., “A vertical model of particle size distributions and fluxes in the midwater column that includes biological and physical processes – Part II: Application to a three year survey in the NW Mediterranean Sea”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 51, pp. 885–908, 2004. [STE 05] STEWART G.M., FOWLER S.W., TEYSSIE J.L. et al., “Contrasting transfer of polonium-210 and lead-210 across three trophic levels in marine plankton”, Marine Ecology Progress Series, vol. 290, pp. 27–33, 2005.

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[STE 07] STEWART G., COCHRAN J.K., MIQUEL J.C. et al., “Comparing POC export from 234Th/238U and 210Po/210Pb disequilibria with estimates from sediment traps in the Northwest Mediterranean”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 54, pp. 1549–1570, 2007. [SZL 09] SZLOSEK J., COCHRAN J.K., MIQUEL J.C. et al., “Particulate organic carbon-Th-234 relationships in particles separated by settling velocity in the Northwest Mediterranean Sea”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 56, pp. 1519–1532, 2009. [TUR 15] TURNER J.T., “Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump”, Progress in Oceanography, vol. 130, pp. 205–248, 2015. [VOL 85] VOLK T., HOFFERT M.I., “Ocean carbon pumps: Analysis of relative strengths and efficiencies in ocean-driven atmospheric CO2 changes”, in SUNDQUIST E.T., BROECKER W.S. (eds), The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present, American Geophysical Union, Geophysical Monograph, 1985. [WHI 88] WHITEHEAD N.E., BALLESTRA S., HOLM E. et al., “Air radionuclide patterns observed at Monaco from the Chernobyl accident”, Journal of Environmental Radioactivity, vol. 7, pp. 249–264, 1988.

3 Zooplankton I. Micro- and Mesozooplankton

3.1. Introduction In this chapter, we begin with a short review of what constitutes the plankton and what in the plankton can be considered as zooplankton, classically considered as animal plankton (in contrast to phytoplankton, the plant plankton). We will show zooplankton to be a very diverse group of planktonic organisms sharing only a particular trophic strategy of relying – at least partially – on the consumption of other organisms. Then, through two sections, each focusing on one of the major types of zooplanktonic taxa (protists and crustacean metazoans), we will attempt to provide an overview of the zooplankton of the Ligurian Sea. 3.1.1. Defining plankton and the different categories of plankton Plankton is a term coined by Victor Hensen to designate “all that drifts in sea”, both living and non-living. Originally, it included everything whose distribution is subject to the currents and movements of water masses. This was everything not attached to, or associated with, bottom surfaces and excludes only swimming organisms, those whose location is not controlled by water movement (e.g. fish, squid). Later, non-living suspended matter was distinguished from live organisms as Seston. Plankton now refers only to living organisms in the water column whose motility is insufficient to overcome currents and movements of water masses. Large-scale physical Chapter written by John DOLAN and Virginie RAYBAUD. The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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displacements of planktonic organisms are passive, due mainly to currents and transport inside moving water masses. In contrast to the plankton are the swimming organisms of the Nekton. Thus, plankton groups organisms share a single characteristic, a relative incapacity to control their locations and displacements in the sea over large scales. It is useful to keep in mind that planktonic organisms are then defined by what they are not capable of, for example, the migrations of salmon or eels, than united by any particular quality. Plankton are typically divided into more or less distinct categories using a variety of non-exclusive criteria. Perhaps the most basic is whether or not an organism is a temporary or permanent member of the plankton. Organisms that are in the plankton for only part of their lifecycle (typically, a larval stage), and the rest commonly spent as a benthic organism, or as a member of the nekton (the swimmers), are in the category of Meroplankton. In contrast to meroplankton are organisms whose entire lifecycles are completed in the plankton, the Holoplankton. The temporary meroplanktonic forms, although of obvious importance to benthic and fish communities, are rarely of significant ecological importance in the plankton and will not be considered in this chapter. Planktonic organisms span a very large range of sizes from that of viruses (nm) to medusa (cm). Size categories are commonly used to divide up the plankton. Thus, planktonic organisms are grouped into the categories of Femtoplankton (< 0.2 µm), Picoplankton (0.2–2 µm), Nanoplankton (2–20 µm), Microplankton (20–200 µm), Mesoplankton (0.2–20 mm) and Macroplankton (2–20 cm). As we will see further on, size is a “master trait” often relatable to fundamental characteristics of average concentration, generation time and swimming speed. Consequently, very different sampling methods and strategies are used to study organisms of the different size classes. However, the size categories do not correspond with other important categorization criteria, such as trophic mode or multi-cellularity. The three major trophic modes found among plankton organisms are autotrophy (self-feeding of organisms, i.e. photosynthesis), heterotrophy (feeding upon another as in consuming others) and mixotrophy in which organisms combine both autotrophy and heterotrophy. Autotrophic organisms of the plankton classically constitute the Phytoplankton (the plant plankton) while heterotrophic organisms, feeding upon others, constitute the Zooplankton (the animal plankton). Mixotrophy complicates

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the appealing simple categorization of organisms as either vegetal or animal. It is important to know that mixotrophy occurs along a gradient of near complete reliance on heterotrophy in some organisms, to near complete reliance on autotrophy in others. Furthermore, a given organism can display “fluidity” or “plasticity” in trophic mode, using different trophic modes depending on prevailing conditions. For a review of mixotrophy among planktonic organisms, see [STO 17]. Only a few of the plankton size categories, the smallest and the largest, can be characterized as grouping organisms of a single trophic mode. The size class containing the smallest taxa, the Femtoplankton, is composed exclusively of viruses infecting other organisms, primarily bacteria, to reproduce themselves and they thus function as heterotrophs. Viruses are found in concentrations of 109 viruses per liter. Like the category for the smallest, the largest size categories are composed almost exclusively of carnivorous, herbivorous and parasitic metazoans all of which are heterotrophic organisms. The other size classes contain organisms of a variety of trophic modes. Picoplankton groups the smallest (0.2–2 µm) cellular organisms. It includes consumers of dissolved organic matter, the heterotrophic prokaryotes (bacteria and archea), along with the smallest of the autotrophs, the autotrophic prokaryotes Synechococcus and Prochlorococcus and diverse small eukaryotic protists. This latter group includes taxa with chloroplasts and carry out photosynthesis, but nevertheless can also ingest prokaryotes, so are thus mixotrophic, as well as taxa that are purely heterotrophic, feeding on a variety of picoplankton. Recent studies have shown that while Synechococcus and Prochlorococcus are primarily autotrophic, some strains are capable of taking up dissolved organic matter (amino acids) and can then be considered mixotrophic. The total concentration of picoplankton cells is commonly about 108 cells per liter with the largest component being that of heterotrophic prokaryotes, representing about 90% of cell numbers. Nanoplankton groups protists, eukaryotic single-celled organisms ranging in size from 2 to 20 µm. The protists include autotrophs (e.g. small diatoms, coccolithophores), heterotrophs (e.g. bacterivorous bodonid flagellates) and mixotrophic taxa (e.g. flagellates with chloroplasts but that also occasionally ingest other organisms). Commonly, nanoplankton concentrations are on the order of 106 cells per liter, about equally divided between heterotrophic cells (mostly bacteriovores) and forms with

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chloroplasts (autotrophs and mixotrophs). The autotrophic and mixotrophic organisms of the nanoplankton generally account for most of the primary production in the plankton. On the consumption side, the heterotrophs and mixotrophs consume the majority of biomass produced by both the autotrophs and the heterotrophs of the picoplankton. The femtoplankton, the picoplankton and the nanoplankton are all essentially microbial composed of viruses, prokaryotes and small protists. While many of the organisms of the picoplankton and nanoplankton are heterotrophic and could be considered as zooplankton (e.g. bacterivorous forms), here we will not further consider organisms of the small size classes, as their exceedingly complex inter-relationships constitute the distinct research domain of microbial ecology. The Microplankton groups organisms ranging in size from 20 to 200 µm. It includes an especially wide variety of taxa: organisms of all three trophic modes and single-celled, multi-cellular as well as colonial forms. Autotrophic taxa include typical phytoplankton such as diatoms and silicoflagellates. Mixotrophic forms are a large variety of protist taxa ranging from phytoplankton-consuming ciliates that sequester chloroplasts from ingested cells to chloroplast-containing dinoflagellates that occasionally ingest other organisms, and radiolarian taxa with symbiotic algal cells embedded in their cytoplasm. Heterotrophs of the microplankton include the strictly heterotrophic protist species of oligotrich ciliates, dinoflagellates, radiolarians which live as individual cells as well as colonial protists such as Zoothanium pelagicum. Heterotrophs among the microplankton also include some metazoans such as nauplii and early copepodite stages of copepods. Total concentrations are generally about 103 organisms per liter. The autotrophic taxa include many forms known to produce dense populations, “blooms” occurring either seasonally (e.g. diatoms) or sporadically (e.g. dinoflagellates). In the cases of blooms, densities may reach 105 organisms per liter. Consumption of phytoplankton by the heterotrophic and mixotrophic components of the microplankton, the microzooplankton, is thought to represent about two-thirds of total daily primary production in most systems. Thus, the microzooplankton are the major herbivores of the marine plankton. The mesoplankton is composed almost exclusively of metazoan taxa; it groups forms ranging in largest dimension from 0.2 to 20 mm. As the organisms of the mesoplankton are very nearly all animal (minor exceptions

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exist such as tufts of the algae Trichodesmium), the mesoplankton is basically synonymous with the term mesozooplankton. It includes the adult stages of the crustacean copepods and cladocera, as well some smaller gelatinous forms such as chaetognaths and appendicularians. The size category also includes some large species of protists, for example phaeodarian radiolaria and the large mixotrophic dinoflagellate Noctiluca. Organismal concentrations are, on average, on the order of 0.5 per liter or 50 organisms per m3 but the density of organisms differs with seasons and among regions. Mesozooplankton feed on a wide range of prey and using a wide range of feeding methods. For example, copepods and cladocerans are often filter feeders, preying preferentially on microplankton, while chaetognaths fed on other mesozooplankton, especially copepods. Mesozooplankton are grazed on by the macrozooplankton and filter feeders of the nekton such as sardines and anchovies. The Macroplankton is composed exclusively of metazoans, all greater than 20 mm in size, so easily seen with naked eye. Because the macroplankton are all animal (a possible exception is Sargassum seaweed may be considered plankton by some) Macroplankton is then largely synonymous with the term Macrozooplankton. It groups relatively large crustacean taxa such as krill and amphipods, as well a very wide range of gelatinous taxa (medusa, ctenophores, siphonophores, salps, etc.). Most macroplankton taxa are either omnivores feeding on mesozooplankton and microplankton, or carnivores feeding on mesoplankton or other macrozooplankton. Some, however, are filter feeders (e.g. salps) and capable of feeding on a wide range of prey items from nanoplankton to mesoplankton. Macrozooplankton are fed upon by taxa within the macrozooplankton, as well as many nekton taxa ranging from sea turtles and sea birds to fish and squid. 3.1.2. Problems with the label zooplankton While zooplankton is often considered to be animal-like plankton, in contrast to phytoplankton as plant-like plankton, we now know that mixotrophy – blurring the division between plant-like and animal-like – is very common. Some taxa typically thought of as zooplankton are indeed undeniably animal-like, with all known species relying completely on the consumption of other organisms or detritus, for example, copepods.

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In other taxa, the majority of species are completely heterotrophic, but mixotrophy is known, for example among medusa with a few species having symbiotic algae. In still other taxa, mixotrophy appears to be nearly the rule rather than the exception, as in the dinoflagellates of the microplankton. Defining zooplankton as planktonic organisms whose nutrition relies in whole or in part on the consumption of pre-formed organic matter is not very satisfactory. It yields a group consisting of the overwhelming majority of organisms and biomass in the plankton as it would include viruses, bacteria, archea, most protist taxa, all metazoa and fungi. Narrowing the definition by specifying consumption of other organisms provides a marginal improvement as it excludes most bacteria and archea. If we attempt a functional definition, for example, defining zooplankton as consumers of primary producers, we still encounter difficulties. Many mixotrophic species are both primary producers and consumers of primary producers. Most consumers of primary producers are omnivores and many preferentially feed on heterotrophic forms; carnivores would be excluded. The problems with the label “zooplankton” are not only semantic, but also conceptual. Quite naturally, we want to catalogue and organize the diversity of the plankton into more or less exclusive categories as the first step in trying to understand the workings of the plankton. The inconvenient truth is that the relationships in the plankton are very far from a simple food chain of primary producers, herbivores, carnivores and top carnivores. Relationships are not well depicted, even as a food web or as a chain. This is because relationships in the plankton such as producer–consumer or competitors for a given resource need not be consistent or constant, but are often variable in time and space. While we know the plankton is characterized by a complexity of relationships and fluidity in trophic modes, nevertheless computer simulations of planktonic communities using relatively few and strictly defined functional groups (e.g. bacteria, bacteriovores, small and large phytoplankton, small and large zooplankton) can successfully mimic observed patterns of abundance in the North Atlantic (e.g. [TAY 93]) and global geographic distributions [STO 14]. The utility of such models using greatly simplified categories suggests that assigning major or dominant functions (e.g. primary producer, herbivore, carnivore) to taxa likely

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reflects reality. Thus, we are left with a less than fully satisfactory (but perhaps fairly accurate) definition of zooplankton as “planktonic organisms on the whole more animal-like than plant-like, with the major function of responsibility for the transfer of autotrophic biomass to higher trophic levels.” 3.2. Ligurian zooplankton 3.2.1. Introduction to microzooplankton and mesozooplankton We have seen that taxa of the zooplankton vary quite widely in size and include an enormous variety of protist and metazoan taxa of seemingly intractable diversity. Some simplification is permissible if not required. Here, we will attempt to foster understanding of the major characteristics of the zooplankton in the Ligurian Sea, through a consideration of a model taxon for two of the major zooplankton categories of microzooplankton and mesozooplankton. The macrozooplankton will not be considered in this chapter, as that extremely diverse group requires a chapter of its own (see Chapter 4). The model taxa presented here are the oligotrich ciliate Strombidium sulcatum (Figure 3.1a) for the microzooplankton and Centropages typicus for the mesozooplankton (Figure 3.1b). The taxa differ considerably in major size-related characteristics (Table 3.1) and the basic characteristic of cellularity. The ciliate is a protist, a single-celled organism, while the copepod is a multi-cellular metazoan. The fundamental differences of cellular organization and body plan are related to large differences in lifecycle and other characteristics which will be detailed in the following sections. Both taxa are strict heterotrophs and follow a typical zooplankton pattern of ingesting food items smaller than their own size. However, there are differences among the taxa with regard to optimal prey size. For ciliates, optimal prey size is about 10% of its size, while for copepods, it is commonly about 1% [WIR 12]. Both taxa are among best-studied taxa of the zooplankton categories of microzooplankton. A simple search using Google Scholar for articles containing the name Strombidium sulcatum yields 570 items, and for Centropages typicus it yields 3,600 items.

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In the following sections, the basic biology of the example taxon will be explained and the major components in the Ligurian Sea of their particular group (microzooplankton, mesozooplankton) will be summarized. Temporal and spatial variability will be considered. These include seasonal changes in abundances and species compositions, differences between near-shore and open water assemblages, and depth-related differences in communities.

Figure 3.1. Model zooplankton taxa: the oligotrich ciliate Strombidium sulcatum (a), the copepod Centropages typicus (b). Drawing credits: (a) D.J.S. Montagnes and (b) T. Kiorboe

Zooplankton Organism

Size (cm)

Swimming Speed (cm s−1)

Swimming Speed Generation (body length s−1) Time (days)

Concentration (organisms per m3)

Oligotrich Ciliate Strombidium sulcatum

0.0004

0.1 (A)

440

0.5

500,000

Copepod Centropages typicus

0.1

3 (B)

30

27

30

Table 3.1. Summary characteristics of model organism of the microzooplankton (ciliate), the mesozooplankton (copepod) and the macrozooplankton (medusa). Note that size is inversely related to swimming speed relative to the size of the organism, generation time and typical concentration. While larger zooplankton taxa swim faster than small taxa in absolute terms, swimming speeds are still very low compared to current velocities (e.g. Ligurian Current of 0.1 m s−1) or typical nekton (e.g. sardines −1 swimming speed of 1 m s ). Swimming speeds relative to the size of the organism differ considerably. Swimming speed sources: (A): [FEN 88]; (B): [CAP 98]

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3.2.2. Sampling 3.2.2.1. Microzooplankton sampling Typically, water sampling bottles (e.g. Niskin or Go-Flo) are used to collect water from a desired depth and an aliquot is preserved with a fixative. A subsample is then settled in a settling chamber and examined using an inverted microscope (Figure 3.2). Plankton nets and pumping systems can be used to sample only for some larger taxa with robust morphologies that resist mechanical damage (e.g. armored dinoflagellates, tintinnid ciliates).

Figure 3.2. Microzooplankton sampling and sample processing. Samples of seawater from a desired depth are obtained using a Niskin bottle. The bottle (1), open at both ends, is lowered to the desired depth, and then the top and bottom lids are closed. The water sample is preserved onboard typically with the iodine-based Lugol’s solution (2). Back in the laboratory, a subsample (usually 100 or 50 ml) of the preserved seawater is left to sediment over a glass-bottom settling chamber (3) for 24–48 hours. The cylinder holding most of the water (all but 3 ml) is slid off the settling chamber (4). The settling chamber is then examined using an inverted microscope (5). Visible in the camera screen image in the upper right is a small tintinnid oligotrich ciliate, and in the lower right a 10 µm white bar. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

3.2.2.2. Mesozooplankton sampling Traditionally, surveys to evaluate planktonic crustacean abundance and diversity used towed nets with mesh sizes ranging from 200 to 680 μm [HAR 00]. The use of WP-II net with 200 µm mesh size is recommended by the UNESCO manual [TRA 68] and is still valid. This is the type of net that has been the most used in the Ligurian Sea since 1955 [RAY 11]. The WP-II (Figure 3.3, left) is a conical simple non-opening/closing 57 cm diameter net (0.25 m² mouth opening; for details, see UNESCO Working Party No. 2 report). The other types of nets that have been commonly used in the region

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present larger mesh sizes and have been used to study large mesozooplankton and macrozooplankton: Juday-Bogorov (330 µm mesh size; Figure 3.3, right), Regent (680 µm mesh size) and BIONESS (500 µm mesh size) [RAY 11]. Sampling is generally performed using vertical, horizontal or oblique hauls.

Figure 3.3. Zooplankton nets. Left: WP-II net. Right: Juday-Bogorov net (pictures: John Dolan)

The sampling design (type of net used, sampling location, sampling frequency, etc.) depends on the objective of the study, the scientific issues to be addressed and the temporal and spatial scales chosen [HAR 00]. In the Ligurian Sea, which is a deep basin, most zooplankton samples have been obtained using vertical or oblique hauls. Vertical hauls are often used with WP-II type nets between 200 m depth (or bottom for coastal samples) and surface. This type of sampling is useful to evaluate the integrated biomass of zooplankton is the surface layer. As zooplankton are known to be often patchily distributed, sometimes, two or three nets are mounted together (BONGO nets) to evaluate the small-scale spatial distribution. Oblique hauls have been often used with multiple opening and closing nets (i.e. BIONESS net [SAM 80]). This multiple net sampling system holds 10 horizontally stacked nets, which open sequentially as one is closed [HAR 00]. This type of instrument is ideal for sampling organisms in discrete water strata and is therefore used to evaluate the vertical distribution and migration of zooplankton (see section 3.4.2.3). Regardless of the type

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of net used, organisms are then generally preserved in approximately 4% formaldehyde solution after sampling, for further taxonomic identification and enumeration. In the last decades, new in situ methods of counting and identification, thus not involved in removing organisms from the water, have been developed such as acoustic or optical counters and underwater video cameras. These instruments of particle characterization and counting are very useful for a rapid high-resolution estimation of zooplankton abundance, but at the cost of a less detailed taxonomic identification than with traditional methods. Acoustical instruments – either fixed on a surface-floating buoy looking downwards or moored near the seafloor looking upwards – record acoustic backscatter returns at multiple ultrasonic frequencies and then provide highresolution information on the distribution and behavior of zooplankton populations [LEM 08]. However, the quantitative interpretation of the acoustic data and accurate classification remains challenging [LAV 10]. Several types of instruments exist but most of them were originally developed for other purposes. For example, acoustic Doppler current profilers (ADCPs), initially used for measuring current velocity, have been adapted to assess zooplankton biomass [SMI 92] whereas echosounders were originally designed to evaluate fish distribution [SUT 05]. Operational optical instruments, such as optical plankton counter (OPC), have also been developed to study zooplankton [HER 88, HER 92]. This remotely towed sensor detects individual particles that pass through the sensing zone and records a digital size unit, proportional to the amount of light blocked by the organism [BEA 99]. An OPC measures the abundance and sizes of zooplankton ranging between approximately 0.25 and 14 mm in equivalent spherical diameter (ESD), and then provides the size distribution of zooplankton samples. Underwater video cameras are systems that take in situ images and videos of zooplankton and particulate matter. The most commonly used system in the Ligurian Sea is the underwater video profiler (UVP; [GOR 00, GUI 08, STE 02, STE 08]). UVP is lowered vertically from a boat and records frames of large particles (> 100 µm) and zooplankton that pass through an illuminated volume of water.

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3.3. The ciliate Strombidium sulcatum and the microzooplankton of the Ligurian Sea 3.3.1. Strombidium sulcatum The review here is based largely on recent summary of work done with Strombidium sulcatum in Villefranche-sur-Mer [DOL 18]. It is a heterotrophic oligotrich, about 40 µm in length, typically cultured using bacteria and small algae as prey. In common with most protists, it generally reproduces asexually via binary fission or cell division. Basic morphological features and stages of cell division in S. sulcatum are shown in Figure 3.4.

Figure 3.4. Gross anatomy and cell division stages of Strombidium sulcatum. Beating of the collar membranelles (CM) moves the cell and brings potential food items to the buccal membranelles for transport into the oral cavity (OC). In the oral cavity, ingested food items are enveloped inside food vacuoles (FV) inside which digestion occurs within the ciliate cell. The macronucleus (MN) is the somatic nucleus and the micronucleus (MN) contains chromosomes replicated during sexual reproduction. During asexual cell division, the daughter cell mouth (DCM) develops in the anterior portion of the cell; the mouth of the parental cell remains functional. The macronucleus is partitioned between the two cells. In the late division stage, the two mouths are functional shortly before cell separation. Adapted from Faure-Fremiet [FAU 12]

3.3.1.1. Swimming, prey capture and excretion Swimming rate and pattern to large extent determine the rate of encountering prey in planktonic consumers. Strombidium sulcatum swims in a helical pattern interrupted by occasional “tumbles” yielding a change of direction [FEN 88, THA 00]. If displacement was consistently in a single

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direction (which it is not), its average swimming speed of about 0.1 cm s−1 would allow it to travel about 100 m in 24 hours. Feeding in an oligotrich like Strombidium sulcatum begins with the capture of the prey item between the collar membranelles (see Figure 3.4). Food items are brought into the oral cavity by the buccal membranelles and food items are isolated in a food vacuole within the ciliate cell for digestion. Prey size, relative to distances between membranelles, influences capture efficiency. In S. sulcatum, the distance between the collar membranelles is about 2 µm [FEN 88] and it feeds most efficiently on items 2–3 µm in size. The maximum filtration rate is about 5 µl per cell per hour. Filtration rates are lower for both small bacteria and large nanoflagellates. However, filtration rates vary considerably among similar-sized bacteria and flagellates, indicating that capture also depends on factors other than size. Prey characteristics that influence prey capture rates in Strombidium sulcatum are the surface characteristics of the potential prey item, small-scale turbulence, and the presence of small detrital particles. Laboratory studies of Strombidium sulcatum provide estimates of the potential grazing impact of oligotrich ciliates. The maximum filtration rate estimate (µl per cell per hour) for S. sulcatum (Figure 3.5), if extrapolated to all oligotrichs, can be used to estimate an aggregate oligotrich community filtration rate, an order of magnitude estimate of the potential impact of oligotrich grazing. In the Bay of Villefranche, oligotrich are usually found in concentrations of about 1,000 l−1 (e.g. [FER 94b, MOS 95]). A filtration rate of about 5 µl per hour per cell yields an aggregate estimate of about 120 ml filtered by oligotrichs found in 1 liter or 12% of the water column filtered per day by oligotrich ciliates in the Bay of Villefranche. Excretion rates of Strombidium sulcatum have been investigated. Nitrogen excretion rates were estimated to be 0.25–2 µg N mg dry weight−1 h−1 [FER 94a] and phosphorus 0–24.6 µg P mg dry weight−1 h−1 [ALL 94]. These rates are relatively high compared to those of metazoan zooplankton, as expected based on known allometric relationships. Interestingly, phosphorus excretion increases with growth rate in contrast to nitrogen excretion, as ammonia [DOL 97]. Ferrier and Rassoulzadegan [FER 94b] in extrapolating nitrogen regenerations measured for S. sulcatum to natural populations of planktonic ciliates in the Mediterranean Sea concluded that ciliates could account for about 25% of total nitrogen regeneration.

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3.3.1.2. Growth Growth has been examined in Strombidium sulcatum feeding on bacteria and a heterotrophic nanoflagellate. Growth rates of up to three generations per day at 15°C were recorded for ciliates grown in relatively dense solutions of bacteria. Growth of S. sulcatum in lower concentrations of bacteria, and growth on a heterotrophic nanoflagellate, were examined by Fenchel and Jonsonn [FEN 88]. In cultures grown at 20°C, the cell division rates, as function of prey concentration, also reached a maximum of about three generations per day for both prey items. The prey concentrations yielding about half the maximum growth rate (1.5 generations per day) were about 1 × 106 bacteria ml−1 or about 5 × 103 nanoflagellate cells ml−1. These concentrations, while higher than those usually recorded for most areas of the Ligurian Sea, are well within the range recorded for the Bay of Villefranche (e.g. [MOS 95]). Based on work with S. sulcatum, oligotrichs in the Ligurian Sea probably reproduce about once a day except perhaps in winter when water temperatures are below 15°C. 3.3.2. Characteristics of the Ligurian Sea assemblages of ciliates While we have focused on Strombidium sulcatum, a mid-sized oligotrich as a representative of ciliate taxa, there are a very large variety of morphotypes among the planktonic ciliates of the Ligurian Sea (Figure 3.5). However, in general terms, smaller-sized forms are more abundant than the larger forms and the most common taxa (80% of cell numbers) are oligotrich ciliates. Small oligotrichs (< 30 µm) are most abundant, found in concentrations of about 700 per liter, medium-sized oligotrichs (30–50 µm) of about 200 per liter and large oligotrichs of about 50 per liter. Total biomass of “small”, “medium” and “large” oligotrichs are often about the same [BER 94, RAS 77]. Mixotrophic oligotrichs represent about half the biomass of oligotrichs. These include the morphologically distinct species of Tontonia and Laboea, as well as about half the species of Strombidium spp. [LAV 88]. Other common non-oligotrich ciliate forms include the raptorial feeding prostome ciliates, capable of ingesting prey as big as themselves, such as Balanion and Didinium, and the mixotrophic Tiarina sp. that harbors symbionts similar to those found in corals [MOR 16], and the nearly autotrophic Mesodinium rubrum (reviewed in [HAN 13]).

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Figure 3.5. Examples of the diversity found among planktonic ciliates of the Ligurian Sea. Oligotrichs: a large Strobilidium-type (A), mixotroph Laboea strobila (B), Strombidium-type oligotrichs of various sizes (C,E,F,G,H,J), and mixotrophic Tontonia-types (D,I). The symbiont-bearing prostomid Tiarina sp. (L), tintinnid Stenosomella ventricosa (M), tintinnid Dadayiella ganymedes (N), prostomid Balanion (O), the predatory ciliate Didinium (K), the mixotrophic haptorid Mesodinium rubrum (P) and a peritrich (Q) perhaps a single cell of Zoothamnium pelagicum. All specimens from the Bay of Villefranche. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

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3.3.3. Seasonal cycles of abundance of ciliates in coastal water Figure 3.6 shows the concentrations in samples integrated throughout the 75 m water column of Point B in the Bay of Villefranche in 2016. Notably, the data show that oligotrichs of different sizes tend to vary together in concentration, except early in the year when the water column structure shifts from vertically mixed to stratified. Total concentrations oscillate around a mean value of about 1,000 cells per liter with no clear seasonal cycle. In contrast, previous studies relying on sampling of near surface waters in the Bay of Villefranche have reported very large temporal variability of ciliate concentrations, and each has reported a different seasonal pattern: December minima and a peak in February [RAS 77], December minima and a peak in July [RAS 88], minimum concentration in March and October and maximum concentrations in August [FER 94a], minimum in May and a peak in October [BER 94], minimum in August and a peak in February [MOS 95], and minimum in March and a peak in April [GOM 03]. The differences likely reflect the fact that near surface concentrations are more variable than concentrations deeper in the water column.

Figure 3.6. Concentrations of planktonic ciliates at Point B, Bay of Villefranche, in 2016 in integrated water column (0–75 m depth) samples. Concentrations were determined by examining material from 100 ml of sample using an inverted microscope. Note that oligotrichs are the dominate group of ciliates and among oligotrichs, the small forms are most abundant. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

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Individual groups of ciliates can show temporal patterns of abundance distinct from the overall community. For example, note that in Figure 3.6, showing data from 2016, tintinnid ciliates showed an early spring peak followed by relatively low and invariant concentrations. A similar pattern was found in a study of tintinnid diversity [DOL 06], based on samples taken at Point B in 2002 and shown in Figure 3.7. Tintinnid ciliates were usually found in abundances of about 20 cells per liter except for an early spring peak, composed largely of Stenosomella spp. Remarkably, despite the relatively low numbers, tintinnid diversity remains high with about 15 species found in material from four liters of an integrated water column sample.

Figure 3.7. Concentrations of tintinnid ciliates at Point B, Bay of Villefranche, in 2002 in integrated water column (0–75 m depth) samples. Concentrations were determined by examining material from four liters of an integrated water column sample using an inverted microscope. Note the distinct peak in late winter/early spring also found in 2016 (Figure 3.9). Despite low average abundances of about 20 cells per liter, diversity is considerable with usually about 15 species present. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

3.3.4. Near-shore to off-shore abundance gradient of ciliates Only one study reported data on ciliate concentrations along a transect in the Ligurian Sea from Nice to Calvi and suggested that ciliate concentrations vary little [RAS 88]. Ciliate abundances at the DYFAMED site (about mid-way between Villefranche and Calvi) were intensively investigated

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in May 1995 [PER 00] and again in September–October 2002 [LAS 11]. In May 1995, both the abundances and portions of mixotrophs compared to strict heterotrophs (about 50%) were similar to those found in the Bay of Villefranche, similar to the findings of Rassoulzadegan et al. [RAS 88]. Based on the May abundance data, ciliate abundances (about 3,000 per liter in the upper 50 m) may be higher in the Ligurian Sea compared to other Mediterranean Seas such as the Catalan Sea (about 400 per liter) and the Adriatic Sea (about 700 per liter). However, it should be kept in mind that the apparent differences may reflect seasonal variability. The sampling in September–October of 2002 yielded concentration estimates of 1,000–2,000 ciliates per liter in the upper 50 m. Furthermore, there is a general pattern in the Mediterranean Sea of higher concentrations of ciliates (and most other components of the plankton) in the Western compared to the more oligotrophic Eastern Mediterranean Sea and a relatively close correlation of chlorophyll a concentrations and ciliate abundances [CHR 11, DOL 02]. 3.3.5. Seasonal variability in abundance of ciliates in off-shore waters and the depth gradient Data on ciliates in off-shore waters of the Ligurian Sea were reported by Tanaka and Rassoulzadegan [TAN 02]. Their study was based on samples taken at the DYFAMED site, the deep-water time-series station located about 50 km off shore of Villefranche, during different seasons. They found large apparent seasonal differences in the concentrations of ciliates in the surface layer (5–75 m depth). Figure 3.8 shows the average concentrations of ciliates in the surface layer. Variability ranged from a winter/autumn minima of 300 to over 2,000 cells per liter in spring, exceeding the variability found in the Bay of Villefranche (Figure 3.8). However, an even greater variability was found to correspond with depth from 5 to 2,000 m. Figure 3.9 shows an overall average depth profile. Near surface concentrations about 1,000 cells per liter, similar to those of the Bay of Villefranche, were found. Concentrations of ciliates decline logarithmically with depth to about 100 cells per liter at 200 m depth and 10 cells per liter at 1,500 m depth. They presented some evidence of depth-related changes in the composition of the ciliate assemblage as average cell size, as equivalent spherical diameter (ESD), differs with depth. Concentrations of the presumed main food resource of ciliates, heterotrophic nanoflagellates, also decreases logarithmically with depth.

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Figure 3.8. Concentrations of ciliates in the surface layer (integrated water column averages 5–75 m) at the DYFAMED (data from Tanaka and Rassoulzadegan [TAN 02]). Note the large temporal differences in concentrations compared to those of the near-shore Point B in the Bay of Villefranche (Figure 3.6)

Figure 3.9. Typical depth-related changes in the concentrations of ciliates and the average size of ciliate cells in the Ligurian Sea at the DYFAMED site (data from Tanaka and Rassoulzadegan [TAN 02])

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3.3.6. Non-ciliate components of the microzooplankton of the Ligurian Sea To our knowledge, there exists very little quantitative data on Ligurian Sea microzooplankton concerning the two major non-ciliate components of the microzooplankton: heterotrophic dinoflagellates and radiolarians. Based on studies conducted in other seas, reasonable expectations can be made with regard to probable concentrations of heterotrophic dinoflagellates. Heterotrophic dinoflagellates are usually as abundant as ciliates based on studies of a wide range of different systems, found in a nearly 1:1 ratio [DOL 05]. Thus, heterotrophic dinoflagellate concentrations are likely about 1,000 cells per liter in the surface waters of the Ligurian Sea. Radiolarian concentrations determined from samples obtained using a 53 µm mesh plankton net at the DYFAMED site in September–October of 2004 were reported by Lasternas et al. [LAS 11]. Radiolarian concentrations in the surface layer (0–90 m) ranging from 1 to 5 cells per liter were found. The concentrations may be underestimated as some species may pass through a 53 µm net. Both heterotrophic dinoflagellates and radiolarians are as morphologically and ecologically diverse as the ciliates. Figure 3.10 shows some heterotrophic dinoflagellates found in the Ligurian Sea. Some species such as Gyrodinium spiralis, Polykrikos kofoidi and Katodinium are known to ingest a wide variety of prey almost as large as themselves. Other forms such as Protoperidinium are assumed to feed primarily on diatoms. For some forms, known to be heterotrophic (as they lack chloroplasts needed for photosynthesis), their nutrition is obscure. These include species of Ornithocercus and Podolampas. In the case of Ornithocercus, the cells usually have symbionts resembling the autotrophic prokaryote Synechococcus. The most abundant group among the radiolarians found in the Ligurian Sea are the nassullarians which have delicate, often intricate silicate shells (Figure 3.11). They feed on small prey items (2–20 µm) using filament-like pseudopodia, extended out the opening of shell, of lengths several times the size of the shell. Symbiotic algae may be found inside the cytoplasm of the radiolarians, suggesting the use of mixotrophy. Some species nearly always have symbionts, other species occasionally are found with symbionts and still others appear to never have symbionts. As with the heterotrophic

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dinoflagellates, the exact nature of the relationship with the symbionts is not known.

Figure 3.10. Examples of heterotrophic dinoflagellates found in the Ligurian Sea. A. Ornithocercus sp.; the golden spheres are symbiotic cyanobacteria whose role in the nutrition of the dinoflagellate is unknown. B. Protoperidinium diabolus feeds using an extra-cellular “feeding veil” to digest prey, often diatoms much larger than itself. C. Podolampas spinifera whose feeding behavior is unknown. D. Gyrodinium spiralis ingests whole prey items. E. Polykrikos kofoidi uses a nematocyst-like organelle to capture prey and draw immobilized prey into the cell; visible in the center of the Polykrikos is an ingested P. diabolus cell. F. Katodinium glaucum (synonym of Lebouridinium glaucum) that feeds using a feeding tube to extract cell contents of prey items. All Lugol’s-fixed specimens are from the Rade de Villefranche, except B & E from the Étang de Thau. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

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Figure 3.11. Examples of radiolarians found in the Ligurian Sea. A. Pterocanium praetextum, a species known to nearly always contain symbiotic algae. B. Paracystidium spiculosum, an enigmatic species of unclear phylogenetic affinity and ecology. C. Arachnocorys circumtexta, known to have symbiotic algae occasionally. D. Corocalyptra sp., E. Pterocorys trochus, known to have symbiotic algae only occasionally. All Lugol’s-fixed specimens are from the Rade de Villefranche. For a color version of this figure, see www.iste.co.uk/migon /mediterranean2.zip

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3.4. The mesozooplankton of the Ligurian Sea and the copepod Centropages typicus as a case study 3.4.1. Presentation of mesozooplankton and ecological role In the global plankton size spectra, mesozooplankton includes drifting planktonic animals of medium size, i.e. ranged between 0.2 and 20 mm. It is a highly diverse group, primarily constituted of small crustaceans, meroplanktonic larvae and (small) gelatinous organisms. Copepods, which are small planktonic crustaceans covered by a chitinous carapace, constitute the dominant group of mesozooplankton with more than 11,000 described species [WAL 19]. The word “copepod” comes from the Greek koipe, which means oar, and podos, which means feet; copepods are equipped with oared legs that serve as feeding tools (mandibles). Also called “ant of the sea”, they have successfully colonized about all the available habitats of the planet, from the surface to the deep sea and from the equator to the poles. Benthic species are also abundant in the microscopic spaces between grains of sediment. As copepods tolerate a large range of salinities, they can be found from freshwater lakes to hypersaline environments. Some of them live freely in the water column (pelagic species), other species inhabit the bottom of the oceans (benthic species) and still others are parasitic copepods (internal or external) of various organisms, from sponges to vertebrates, including fish and marine mammals. The morphology of parasitic copepods is largely different from free-living ones: short antenna, appendages reduced, strongly modified or absent. Some species of copepods parasitize fish skin and gills and cause substantial economic loss for both fisheries and aquaculture. Whereas some copepod species are strict carnivores, most of them are omnivorous and are able to switch from vegetal to animal or even detritus food sources (Figure 3.12) [ALC 03]. Regardless of their diet, they are able to select the particle they catch using size, chemical composition and nutritional quality, ingesting only chosen items. Such selective feeding allows them to avoid toxic species and to optimize the ratio between the gain of energy and the loss associated with the assimilation of the prey [MOL 13]. The reproduction of copepods occurs by mating, and individuals are either female or male. Unlike many aquatic species that release the gametes directly into the water, males locate females by following their pheromone

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trails in the water and then hold them with their antennas. A copepod male is able to locate a female from a distance of 10 cm, which is more than 100 times its own size (for a human-sized animal equal to about 200 m!). Once the female is located, the male approaches and clings to the abdomen of the female using his fifth pair of legs which are modified like a hook. Once fertilized, eggs are, depending on the species, released into the water or carried by the female in one or two ovigerous bags under her abdomen. The fecundity of copepods is generally of the order of a few tens to a few hundred eggs per female per day [MOL 13].

Figure 3.12. (a) Candacia simplex (carnivorous, body length: 1,800 µm). (b) Oithona similis (predator of protozoa, body length: 700 µm). (c) Clausocalanus arcuiconis (herbivore, body length: 1,200 µm). Credit: Stéphane Gasparini. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

After copepods, the second most important group is euphausiids. These shrimp-like organisms are well-known in high latitudes (Arctic and Antarctic waters) as krill, on which whales, seals and penguins feed. However, euphausiids are also present in all basins of the global ocean, including

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the Ligurian Sea. For example, the northern krill Meganyctiphanes norvegica is known to inhabit a wide range of habitats, from Arctic waters to the Mediterranean Sea [MAU 80, MAY 99]. This species is an important element of the pelagic food web as a trophic resource for fish, birds and whales in many regions of the world ([LAB 96, PEA 79], see Chapter 4). The other groups of holo-mesozooplankton are the mysids, cladocera, ostracods, cumaceans, amphipods, isopods and small-size gelatinous organisms. 3.4.2. Characteristics of the Ligurian Sea assemblages of crustacean zooplankton 3.4.2.1. Annual cycle and short-term changes Over an annual cycle, crustacean zooplankton as a whole exhibit a seasonal cycle with a strong increase in abundance that typically occurs during spring (from February to May), just after the phytoplankton bloom, on which most of these organisms feed (Figure 3.13). The composition of mesozooplankton also show substantial changes over one year, with a dominance of calanoid copepods during the spring peak while the relative abundance of other taxa such as cladocerans and appendicularians increases just after [GOR 10].

Figure 3.13. Annual cycle of abundance (ind.m−3) of total copepods, calculated with data collected weekly at point B (Villefranche-sur-Mer) from 2005 to 2010 (mean and standard deviation). Data: [OLI 15]

Variations of the mesozooplankton community structure is also coupled to hydrodynamic processes that occur at a short time scale. For example, Andersen et al. [AND 01a, AND 01b] studied the effect of the transition

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from spring bloom to oligotrophy on zooplankton communities with a sampling strategy that consisted of two net-hauls per day (one during daytime and one during nighttime) for three weeks. During this period, the decline of the overall abundance of copepods was associated with an increase in the relative abundance of carnivorous organisms (copepods Euchaeta acuta, Heterorhabdus spp. and euphausiids Nematoscelis megalops and Stylocheiron longicorne).

Figure 3.14. Temporal variation of total copepods abundance sampled with (a) WP-II net and (b) BIONESS net, during DYNAPROC 2 cruise (September–October 2004). Dashed lines: day data; continuous lines: night data. In gray: data from frozen samples. In blue: percentage of the 0–200 m water column occupied by low-salinity water (LSW, < 38.30). (c) Temporal variation of the Shannon’s diversity index calculated on large copepods data (from Raybaud et al. [RAY 08a]). For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

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The seasonal shift in mesozooplankton community composition was also investigated during the summer–autumn transition [RAY 08a, RAY 09]. The studies showed that intrusions of coastal low-salinity water masses, containing their own zooplankton community, could occur in the central part of the Ligurian Sea, which was thought to be isolated from the coast by the Ligurian front [BET 83]. These lenses of low-salinity water contained their own zooplankton community, with higher abundances of some groups: Nannocalanus minor, Neocalanus gracilis, Euchaeta acuta, Mesocalanus tenuicornis [RAY 08a]. Notably, night and day abundances of total copepods were higher during LSW intrusion, both with WP-II and BIONESS nets and large copepod diversity (Shannon index) decreased (Figure 3.14). 3.4.2.2. Near-shore to off-shore abundance gradient of crustacean zooplankton The distribution of crustacean zooplankton from the coast to offshore waters of the Ligurian Sea follows the hydrological patterns that exist in this region. The Ligurian current is responsible for the presence of a permanent geostrophic front, associated with numerous mesoscale processes that lead to intense meanders, filaments and eddies. This frontal structure acts as a barrier restraining lateral input of particles from the coast into the central zone and separates the area into three distinct parts: coastal, frontal and central (offshore) zones [PRI 81]. The Ligurian front has been reported to have a significant effect on zooplankton distribution and the assemblages of species are different in each of the three zones. For example, Boucher et al. [BOU 87] found that the copepods Temora stylifera, Centropages typicus, Euterpina acutifrons, Candacia spp., Corycaeus spp., chaetognaths, cladocerans and echinoderm larvae had a coastal distribution. In contrast, Calanus helgolandicus and Clausocalanus spp. were found to have an offshore distribution [BOU 84]. The frontal water masses appeared to be a highly suitable habitat for the development of mesozooplankton populations. Frontal upward advection supports a high primary production, stimulating trophic transfers throughout the entire pelagic food web. During the 1980s and the 1990s, several sampling campaigns examined the frontal zone, where high densities of copepods have been reported, associated with enhanced feeding conditions [BOU 84, BOU 87, IBA 87, ZAK 98]. More recently, Licandro and Icardi [LIC 09] found similar results during an oceanographic campaign that

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covered the whole eastern part of the Ligurian Sea, at the end of autumn. They recorded the greatest values of biomass and abundance in the frontal zone and found a dominance of the copepods Clausocalanus spp. (46% of total zooplankton) and Oithona spp. (15%). 3.4.2.3. Vertical distribution and diel migrations An overview of diel vertical migration is given in Box 3.1. In the Ligurian Sea, the diel vertical migration of zooplankton has been relatively well documented over the last 30 years [AND 01b, AND 92, RAY 08b, SAR 96]. Most of these studies showed that the majority of zooplankton species appear to be migrators, with a migration distance of more or less large amplitude depending on the species (e.g. 155 m as a mean for the mysid Eucopia unguiculata and up to 630 m for the decapod Gennadas elegans [SAR 93]). In contrast, other species such as the euphausiid Stylocheiron longicorne has been reported to be non-migrant by all these studies.

Figure 3.15. Night and day vertical distribution of the main crustacean migrant species, sampled in the central part of the Ligurian Sea, during the DYNAPROC 2 cruise in September–October 2004. Meganyctiphanes norvegica (euphausid), Nematoscelis megalops (euphausid), Vibilia armata (hyperid amphipod). Adapted from Raybaud [RAY 08b]. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

Figure 3.15 shows night and day vertical distribution of the main crustacean migrators, sampled in the central part of the Ligurian Sea, during the DYNAPROC 2 cruise (September–October 2004). Among the species with an herbivorous tendency, the most abundant migrant was the euphausiid Meganyctiphanes norvegica. This species was located between 0 and 150 m depth during nighttime, with a maximum between 25 and 75 m, where the deep chlorophyll maximum was located. During the day, M. norvegica

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moves down to a 450–550 m depth. Among carnivorous organisms, the most abundant migrants were the euphausiid Nematoscelis megalops and the hyperiid Vibilia armata. Unlike the herbivores, these predatory organisms swim upward and downward to follow their prey. The euphausiid N. megalops was mainly located between 75 and 150 m depth at night and between 450 and 550 m depth during the day. At night, V. armata was the most abundant in the superficial layer (0–25 m depth) and then found at depth back during daytime (550–700 m depth). Despite their quite limited swimming capacity and their relatively small size, most of zooplanktonic organisms perform night-day vertical migration that can reach several hundreds of meters. Diel vertical migrations occur in all regions of the world and are possibly the largest daily migration by biomass in the natural world [BRI 14]. At nighttime, organisms swim towards the surface layer to feed on phytoplankton and return to the epipelagic layer during day to avoid predators that hunt at sight (Figure 3.16). The most important trigger for diel vertical migration seems to be changes in light intensity [DAA 68, SIE 60], although other factors, such as food concentration, distribution of predators or physical barriers, also influence the vertical distribution of organisms [HAY 03, ISL 15, PEA 03]. Vertical migrations contribute to the biological pump by actively and quickly transporting the organic carbon from surface layer to deep waters [STE 00].

Figure 3.16. Schematic representation of the diel vertical migration of copepods. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip Box 3.1. Diel vertical migration

3.4.3. Centropages typicus, a dominant copepod species in the Ligurian Sea 3.4.3.1. Distribution and ecology Centropages typicus (Figure 3.17) is one of the best-known copepod species in terms of its biology, physiology and ecology. It is a common calanoid copepod with a large geographical distribution. It is found in

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temperate waters from the Mediterranean Sea to the northern part of the Atlantic Ocean, along Norwegian coasts [BEA 07]. In the Mediterranean Sea, it is one of the seven species of Centropages recorded by Rose [ROS 33]: C. typicus, C. chierchiae, C. kroyeri, C. violaceus, C. bradyi, C. aucklandicus and C. hamatus. It is a neritic-coastal species that mainly occurs over continental shelves and shallow estuaries, although it can be occasionally recorded in oceanic regions, near continental slopes [BEA 07, CON 04]. It has been hypothesized that its usual restriction to coastal waters is related to a relatively poor capacity to tolerate long-term food limitations [DAV 92]. Variability in concentrations is thought to be mainly driven by temperature, as well both quantity and quality of the available food [BEA 07].

Figure 3.17. Adult female of Centropages typicus (body length: 1,600 µm). Credit: Stéphane Gasparini. For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

Centropages typicus is an omnivorous copepod, feeding on a large spectrum of organisms, from small unicellular microalgae [TOM 78] to fish larvae [CAL 07, TUR 85]. Microzooplankton, and especially the ciliate Strombidium sulcatum, is also an important part of C. typicus diet. For example, Wiadnyana and Rassoulzadegan [WIA 89] showed in a laboratory study that, when a ciliate + phytoplankton mixture is offered to C. typicus,

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the copepod actively selects ciliates to feed on (80% of the ingested ration). Moreover, it has also been reported that C. typicus can also feed on juveniles and eggs of appendicularians as well as on nauplii of other copepods [CAL 07]. To capture prey, C. typicus is able to switch between two feeding behaviors: ambush feeder and suspension feeder strategies [TIS 90]. When feeding on small particles, the copepod adopts a suspensivore, filter feeding mode, generating a feeding current. For larger prey, it uses an ambush strategy, passively waiting for their prey motionless in the water and catching them by fast surprise attacks [CAL 07, KIØ 09]. 3.4.3.2. Lifecycle of Centropages typicus The lifecycle of Centropages typicus follows the classical lifecycle of most copepods. It includes 12 different stages after egg; each stage being separated by molts (Figure 3.18). The first six larval stages are named “nauplii” (abbreviated NI to NVI) and the following five stages are named “copepodits” (CI to CV); the 12th stage being the adults. Identification of the successive stages of development is based on the number of free somites or distinct body sections and number of pairs of swimming legs. The length of the lifecycle is about one month. However, in other copepod species, it can vary from one week to as long as one year. Development is also strongly influenced by environmental factors, mainly seawater temperature and the amount of available food.

Figure 3.18. Schematic lifecycle of Centropages typicus. Larval development involves six naupliar stages (NI to NVI) and five copepodits stages (CI to CV). For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

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3.4.3.3. Centropages typicus in the Ligurian Sea Centropages typicus is present in the whole Mediterranean Sea and constitutes an important part of the copepod community, particularly in the north-western part of the basin. During spring, this species dominates the coastal communities, representing 65 to 70% of total copepods number in the Ligurian Sea [GAU 62, RAZ 72]. Mazzocchi et al. [MAZ 07] compared the interannual patterns of C. typicus abundance at five sites over the Mediterranean Sea (Balearic Sea, Bay of Villefranche, Gulf of Naples, Gulf of Trieste and Saronikos Gulf) and showed that the highest values were recorded in the Bay of Villefranche. Longitudinally, the abundance of C. typicus decrease from west to east, and it is nearly absent in the oligotrophic Levantine Sea [LAK 90]. C. typicus is essentially found in surface layers, between 0 and 150 m [AND 01b, SCO 84]. The species exhibits a narrow daily vertical migration between the maximum chlorophyll peak and the surface [SAI 90].

Figure 3.19. Annual cycle of the abundance (individuals.m−3) of Centropages typicus in 1999 in the Ligurian Sea (data from Molinero [MOL 03])

Over an annual cycle, Centropages typicus in the Ligurian Sea exhibits a marked seasonal cycle, with low abundances during winter and a major peak between March and June. This is earlier than what is observed in the Atlantic Ocean [MAZ 07]. During this period, the abundance of the copepod can reach values higher than 350 ind.m−3 in the Ligurian Sea (Figure 3.19).

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During summer and autumn, the abundance of C. typicus declines to 5–10 ind. m−3, whereas the reproduction rate is optimal. During this period, the population is regulated through hatching and the development of young stages probably depends on the heterotrophic elements of the microbial food web as prey [MOL 03]. The annual cycle is a succession of five to seven generations [HAL 01, RAZ 74]. As C. typicus has no lipid reserve, its fecundity rate is conditioned by the quantity and quality of the food in near real time, and egg production rates can vary between 36 and 100 eggs female−1 day−1 in the Northwestern Mediterranean Sea [HAL 01]. Long-term phenological changes in C. typicus populations have been observed in the Bay of Villefranche from 1966 to 1993. These fluctuations have been related to large-scale climate variations, especially the North Atlantic Oscillation (NAO). During positive phases of winter NAO, the region experienced a milder and dryer climate and the abundance of C. typicus was higher, with a bimodal annual cycle. At the opposite, during negative phases of NAO, observations showed lower abundances and a unique and reduced spring peak [MOL 05]. 3.5. References [ALC 03] ALCARAZ M., CALBET A., “Zooplankton ecology”, in DUARTE C. and LOTT HELGUERAS A. (eds), Marine Ecology. Encyclopedia of Life Support Systems (EOLSS), Eolss Publishers, Oxford, Developed under the Auspices of the UNESCO, 2003. [ALL 94] ALLALI K., DOLAN J., RASSOULZADEGAN F., “Cuture characteristics and orthophophate excretion of a marine oligotrich ciliate, Strombidium-sulcatum, fed heat-killed bacteria”, Marine Ecology Progress Series, vol. 105, pp. 159–165, 1994. [AND 92] ANDERSEN V., SARDOU J., “The diel migrations and vertical distributions of zooplankton and micronekton in the Northwestern Mediterranean Sea. 1. Euphausiids, mysids, decapods and fishes”, Journal of Plankton Research, vol. 14, pp. 1129–1154, 1992. [AND 01a] ANDERSEN V., NIVAL P., CAPARROY P. et al., “Zooplankton community during the transition from spring bloom to oligotrophy in the open NW Mediterranean and effects of wind events. 1. Abundance and specific composition”, Journal of Plankton Research, vol. 23, pp. 227–242, 2001.

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[AND 01b] ANDERSEN V., GUBANOVA A., NIVAL P. et al., “Zooplankton community during the transition from spring bloom to oligotrophy in the open NW Mediterranean and effects of wind events. 2. Vertical distributions and migrations”, Journal of Plankton Research, vol. 23, pp. 243–261, 2001. [BEA 07] BEAUGRAND G., LINDLEY J.A., HELAOUET P. et al., “Macroecological study of Centropages typicus in the North Atlantic Ocean”, Progress in Oceanography, vol. 72, pp. 259–273, 2007. [BEA 99] BEAULIEU S.E., MULLIN M.M., TANG V.T. et al., “Using an optical plankton counter to determine the size distributions of preserved zooplankton samples”, Journal of Plankton Research, vol. 21, pp. 1939–1956, 1999. [BER 94] BERNARD C., RASSOULADEGAN F., “Seasonal variations of mixotrophic ciliates in the northwest Mediterranean sea”, Marine Ecology Progress Series, vol. 108, pp. 295–301, 1994. [BET 83] BÉTHOUX J.-P., PRIEUR L., “Hydrologie et circulation en Méditerranée nord-occidentale”, Pétroles et techniques, vol. 299, pp. 25–34, 1983. [BOU 84] BOUCHER J., “Localization of zooplankton populations in the Ligurian marine front: Role of ontogenic migration”, Deep-Sea Research Part A – Oceanographic Research Papers, vol. 31, pp. 469–484, 1984. [BOU 87] BOUCHER J., IBANEZ F., PRIEUR L., “Daily and seasonal variations in the spatial distribution of zooplakton populations in relation to the physical structure in the Ligurian sea front”, Journal of Marine Research, vol. 45, pp. 133–173, 1987. [BRI 14] BRIERLEY A.S., “Diel vertical migration”, Current Biology, vol. 24, pp. R1074–R1076, 2014. [CAL 07] CALBET A., CARLOTTI F., GAUDY R., “The feeding ecology of the copepod Centropages typicus (Kröyer)”, Progress in Oceanography, vol. 72, pp. 137–150, 2007. [CAP 98] CAPARROY P., PEREZ M.T., CARLOTTI F., “Feeding behaviour of Centropages typicus in calm and turbulent conditions”, Marine Ecology Progress Series, vol. 168, pp. 109–118, 1998. [CHR 11] CHRISTAKI U., VAN WAMBEKE F., LEFEVRE D. et al., “The impact of anticyclonic mesoscale structures on microbial food webs in the Mediterranean Sea”, Biogeosciences Discussions, vol. 8, 2011. [CON 04] CONTINUOUS PLANKTON RECORDER SURVEY T., “Continuous plankton records, plankton atlas of the North Atlantic Ocean (1958–1999). II. Biogeographical charts”, Marine Ecology Progress Series, pp. 11–75, 2004.

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[ISL 15] ISLA A., SCHAREK R., LATASA M., “Zooplankton diel vertical migration and contribution to deep active carbon flux in the NW Mediterranean”, Journal of Marine Systems, vol. 143, pp. 86–97, 2015. [KIØ 09] KIØRBOE T., ANDERSEN A., LANGLOIS V.J. et al., “Mechanisms and feasibility of prey capture in ambush-feeding zooplankton”, Proceedings of the National Academy of Sciences of the United States of America, vol. 106, pp. 12394–12399, 2009. [LAB 96] LABAT J.P., CUZIN-ROUDY J., “Population dynamics of the krill Meganyctiphanes norvegica (M Sars, 1857) (Crustacea: Euphausiacea) in the Ligurian Sea (NW Mediterranean sea). Size structure, growth and mortality modelling”, Journal of Plankton Research, vol. 18, pp. 2295–2312, 1996. [LAK 90] LAKKIS S., “Composition, diversity and successions of planktonic copepods in the Lebanese waters (Eastern Mediterranean)”, Oceanologica Acta, vol. 13, pp. 489–501, 1990. [LAS 11] LASTERNAS S., TUNIN-LEY A., IBANEZ F. et al., “Short-term dynamics of microplankton abundance and diversity in NW Mediterranean Sea during late summer conditions (DYNAPROC 2 cruise; 2004)”, Biogeosciences, vol. 8, pp. 743–761, 2011. [LAV 88] LAVAL-PEUTO M., RASSOULZADEGAN F., “Autofluorescence of marine planktonic Oligotrichina and other ciliates”, Hydrobiologia, vol. 159, pp. 99–110, 1988. [LAV 10] LAVERY A.C., CHU D., MOUM J.N., “Measurements of acoustic scattering from zooplankton and oceanic microstructure using a broadband echosounder”, Ices Journal of Marine Science, vol. 67, pp. 379–394, 2010. [LEM 08] LEMON D.D., BILLENNESS D., BUERMANS J. et al., “Comparison of acoustic measurements of zooplankton populations using an acoustic water column profiler and an ADCP”, in Oceans 2008, Vols 1–4, 2008. [LIC 09] LICANDRO P., ICARDI P., “Basin scale distribution of zooplankton in the Ligurian Sea (north-western Mediterranean) in late autumn”, Hydrobiologia, vol. 617, pp. 17–40, 2009. [MAU 80] MAUCHLINE J., “The biology of mysids and euphausiids”, in Advances in Marine Biology, Vol. 18, Academic Press, London, 1980. [MAY 99] MAYZAUD P., VIRTUE P., ALBESSARD E., “Seasonal variations in the lipid and fatty acid composition of the euphausiid Meganyctiphanes norvegica from the Ligurian Sea”, Marine Ecology Progress Series, vol. 186, pp. 199–210, 1999.

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[MAZ 07] MAZZOCCHI M.G., CHRISTOU E.D., DI CAPUA I. et al., “Temporal variability of Centropages typicus in the Mediterranean Sea over seasonal-to-decadal scales”, Progress in Oceanography, vol. 72, pp. 214–232, 2007. [MOL 03] MOLINERO J.C., Etude de la variabilité des abondances des copépodes planctoniques en Mediterranée, mécanismes et échelles caractéristiques: le cas de Centropages typicus, Thesis, Université Pierre et Marie Curie, Paris VI., 2003. [MOL 05] MOLINERO J.C., IBANEZ F., NIVAL P. et al., “North Atlantic climate and northwestern Mediterranean plankton variability”, Limnology and Oceanography, vol. 50, pp. 1213–1220, 2005. [MOL 13] MOLLO P., NOURY A., Le manuel du plancton, Éditions Charles Léopold Mayer, France, 2013. [MOR 16] MORDRET S., ROMAC S., HENRY N. et al., “The symbiotic life of Symbiodinium in the open ocean within a new species of calcifying ciliate (Tiarina sp.)”, Isme Journal, vol. 10, pp. 1424–1436, 2016. [MOS 95] MOSTAJIR B., DOLAN J.R., RASSOULZADEGAN F., “Seasonal variations of pico- and nano-detrital particles (DAPI Yellow Particles, DYP) in the Ligurian Sea (NW Mediterranean)”, Aquatic Microbial Ecology, vol. 9, pp. 267–277, 1995. [OLI 15] OLIVIER M., PREJGER F., GASPARINI S. et al., “Temporal evolution of zooplankton from 2004 to 2010 from WP2 net in the Northwestern Mediterranean Sea”. Available at: https://doi.org/10.15468/xwmazu, 2015. [PEA 79] PEARCY W.G., HOPKINS C.C.E., GRONVIK S. et al., “Feeding habits of Cod, Capelin, and Herring in Balsfjorden, northern Norway, July–August 1978 – Importance of Euphausiids”, Sarsia, vol. 64, pp. 269–277, 1979. [PEA 03] PEARRE S., “Eat and run? The hunger/satiation hypothesis in vertical migration: History, evidence and consequences”, Biological Reviews, vol. 78, pp. 1–79, 2003. [PER 00] PEREZ M.T., DOLAN J.R., VIDUSSI F. et al., “Diel vertical distribution of planktonic ciliates within the surface layer of the NW Mediterranean (May 1995)”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 47, pp. 479–503, 2000. [PRI 81] PRIEUR L., “Hétérogénéité spatio-temporelle dans le bassin liguroprovençal”, Rapp. Comm. Int. Mer Méd., vol. 27, pp. 177–179, 1981.

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4 Zooplankton II. Macroplankton and Long-Term Series

4.1. Macroplankton: the large planktonic animals 4.1.1. Overview of the size class The macroplankton size class (2–20 cm) contains a large variety of species from diverse taxonomic groups that have very different functional roles in the dynamics of the pelagic food web: micro-feeders, cruising and ambush predators, web feeders, etc. Many of them have a gelatinous structure adapted to this pelagic environment without shelter, being transparent and light. The concept of “gelatinous plankton” was created to group together some of these morphologically disparate animals [HAM 75], which naturally contain a high amount of water [KIØ 13, MCC 17]. Some of their characteristics are given below. An illustration of some macroplankton species was given by Vandromme [VAN 11] from scans of plankton samples sorted and counted via the ZooScan method. Figure 4.1 shows the high variety of aspects among macroplankton. The species with a dimension greater than 20 cm are considered megazooplankton; this term has been coined to group all the largest plankton species. However, most of these large animals have larvae and juveniles smaller than adults. Therefore, it is necessary to consider these early life stages as meso- or macrozooplankton. For this reason, we pool “macro” and “mega” zooplankton and consider here that the “macrozooplankton” size class covers two orders of magnitude (2 mm–200 cm). It should be kept in mind that these size categories are Chapter written by Paul NIVAL, Fabien LOMBARD, Janine CUZIN, Jacqueline GOY and Lars STEMMANN. The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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based on the diameter of a sphere of the same volume as the individuals. The shape of most of the macroplankton species deviates from a sphere.

Figure 4.1. Aspect of different species from plankton net samples scanned with the ZooScan method (Gorsky et al. 2010), in Vandromme [VAN 11]. All these pictures are at the same scale (given at bottom right: 5 mm), except the “small Copepods” in the upper left corner (1 mm segment). Most of these species, growing in size from larvae and juvenile to adult stages, will increase in size from one to two orders of magnitude. A few species aggregate as chains or colonies, reaching very large sizes [VAN 11]

Dynamics of the main zoological groups in the Ligurian Sea is introduced in the following. 4.1.2. Mollusks (Gastropoda) Pelagic mollusks belong to the gastropod class. Only a small number of pelagic species have the coiled shell, typical of this group. Nearly all pelagic mollusk species have no shell or only a reduced and lightly calcified one. In some species, the transparent shell is large enough to let the animal retract into this narrow shelter. The recoiling of shelled species, withdrawn into their shells, is an escape behavior when disturbed. The absence of a shell appears to be advantageous to stay and move in the superficial productive layers of the sea. Most of the species migrate every night from the mesopelagic depth to the surface in order to feed. During the day, adults are

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located deeper than early stages of many planktonic species. As many other kinds of mollusks, pelagic ones are hermaphrodites and need to mate to reproduce. These mollusks do not crawl but swim or “fly” in the water. Their foot is flattened as two wings (pteropod group) or as a paddle (Littorinomorpha group = heteropod). Pteropods are microphagous, particle feeders [CON 18], except Gymnosoma, which are predators of other pteropods. Heteropods are carnivorous. 4.1.2.1. Pteropods The name pteropod comes from the foot that they use to swim, showing two paddles (fins) that resemble butterfly wings. Euthecosoms pteropods have a “real” shell (eu = real; thecosoms = shells surrounding their body) while their foot is converted in wings (ptero = wings, podos = foot). Thecosoms are particle feeders (herbivorous and detritivores). Common Genus: Limacina, Creseis, Cavolinia, less common: Hyalocylis, Euclio. They are capable of nychthemeral migration that has been recorded in the Ligurian Sea between the surface and 300–600 m depths during daytime [AND 92, SAR 93], which may lead to partial underestimation of adult abundances by diurnal sampling in surface waters. Yonge [YON 26] sampled pteropods in the Bay of Villefranche and showed, with careful observations, that the ciliated surface of parapods carries particles to their mouth. However, the main feeding process was discovered by in situ observations [GIL 74]. These mollusks produce mucous filaments that aggregate to form a mucous veil on which are collected particles sedimenting in the water column. The mucous veil is able to retain particles larger than 15 µm [GIL 74]. The density of mucus being less than that of seawater density, the animal can rest suspended with this parachute float. From time to time, the mucus is ingested with its catch of particles and a new mucous web is secreted. When disturbed, the pteropod detaches from the mucous web and falls down to escape the predator. Some pteropod species forming such dense aggregations or blooms that sedimenting shells from dead individuals accumulate on the bottom. Such layers of pteropod shells can be observed in sediment cores [BIE 89]. The analysis of a time series of the abundance of pteropods suggests a long-term oscillation of abundance, parallel to the summer temperature 14-

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year period variation, suggesting the influence of climate conditions illustrated by the North Atlantic Oscillation [HOW 15]. Pseudothecosomes species have no shell but they have a cartilaginous pseudo shell that protects their body. This provides them with some buoyancy. Their foot is transformed into two large wings. Very often, transparent pseudo shells of Cymbulia separated from the animal are found on Ligurian beaches. Gymnosome pteropods are small mollusks without a shell (gymno = nude; soma = body) that are considered as specific predators of the thecosom pteropods. Due to their reproduction process, pteropods form patches with high concentrations of adults and with the production of abundant egg groups in mucous webs. This behavior favors their predators, especially gymnosomes. Because of their hydrodynamic shape, these species are able to swim rapidly and, when in contact with their prey, they evaginate a long proboscis equipped with suckers. The secured prey is rapidly eaten. Sentz-Braconnot [SEN 65] collected individuals of Pneumodermopsis during a bloom of the Thecosome Creseis in the Bay of Villefranche. She suggested that gymnosomes select their prey. 4.1.2.2. Littorinimorpha mollusks Littorinimorpha mollusks are also known under the name heteropods because their foot shows a single paddle (fin). Their body is transparent except the black reflecting part of the digestive tract and the eyes. The shape of their radula suggests that these animals are carnivorous. A few species have a coiled shell (Atlanta) or a very small one set over digestive glands, gill and reproductive parts (Carinaria). Other species have no shell. Their spatial distribution, lifecycle and predatory impact are not known in the Ligurian Sea. From Russian time series [MOR 85], Pterotrachea is frequently observed in the Bay of Villefranche during the winter and spring (December to May). 4.1.3. Annelids Pelagic annelids belong to the group Polychaeta, Errantia. Among them two groups of species should be considered. First, large species. They are long animals of Nereis shape that swim rapidly. They are able to escape

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plankton nets and, if caught, they appear in samples as broken pieces. The most frequent genera are Torrea, Callizona, which have well-developed eyes. They are carnivorous. Second, small-sized species. Some have paddle like parapods but a short body. The elegant genus Tomopteris has characteristic bi-lobate parapodia. Smaller species from genera (Pelagobia, Lopadorrhynchus and Typhloscolex) are not collected by large-mesh nets commonly used to collect macroplankton. They appear unbroken in WPII samples (mesh 200 µm) and can reach densities of 10 individuals per 100 m3 [PIN 95]. There is nearly no information, no data, on the ecology of these carnivores in the Ligurian Sea. 4.1.4. Chaetognaths At first glance, these organisms (arrow worms) all appear to have the same shape: an elongated body like an arrow and large setae-like hooks around the mouth. However, careful observation shows that there are differences among species and genera with regard to transparent fins, eyes and setae. The digestive track is linear from mouth to anus, which opens at some distance from the tail, a large nervous patch in the middle of the body and paired gonads, male and female, separated by septa at the rear part of the body. Chaetognath species are predators of copepods. They are ambush predators that float steadily most of the time and then suddenly jump to catch a prey. It has been suggested that chaetognaths detect their prey by the vibrations they produce when they are feeding. In the Bay of Villefranche, three species are common. Sagitta setosa is abundant during summer (47.3% of the collected individuals in weekly samples over one year); Sagitta minima appears at the end of autumn and winter (31.2%); and S. enflata appears during summer. Pooling all species, the abundance of chaetognaths in the surface layer (0–75 m) is higher than six individuals m−3 at the end of summer, the end of autumn and start of winter [IBA 69]. Common species in deep water of the Ligurian Sea are Sagitta lyra, S. serratodentata and Pterosagitta draco. Dallot [DAL 68] managed to raise Sagitta setosa in the laboratory. Reproduction is rapid. Ovaries develop in a few days. Large ovules are spawn at sunrise every day if the animal is well fed (average: 16 per spawning period). Auto-fecundation is possible. Embryonic development

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proceeds inside egg envelope. It gives rise to 800 µm-long larvae of adult aspect in 19 hours, at 21°C. Several species of predators are ambush predators, waiting for their prey, so the vertical migration of prey or predators mediated by the variation in light intensity must be the main factor for carnivore dynamics. 4.1.5. Planktonic prochordates – tunicates 4.1.5.1. Appendicularians These microphagous animals feed on nano- and picoplanktonic cells. They produce special filters of complex architecture usually called a “house” that surround the animal and into which the animal actively pumps water. This mucous house is secreted by special cells from the external pharyngeal epidermis [FEN 98a, FEN 98b] that shows a complex and precise spatial pattern. The size of the house is 5 mm for species from surface waters to 10 cm for species observed at 350 m during dives in the Ligurian Sea. These animals are stationary when feeding, so they might be vulnerable to predators. When disturbed, the animal jumps out of its house and soon produces another one. The same behavior is observed when the filters are clogged. The animal inflates a new house that was produced previously, folded on its supra-pharyngeal epidermis. They swarm to be close to one another in order to reproduce by shedding their gametes in the water. The mature gonad wall breaks at reproduction; therefore, the adult dies thereafter. A consequence is that for these species, generation time is equal to lifetime. Two genera are common in surface waters: Oikopleura and Fritillaria [FEN 68]. Fritillaria is more common during winter, and Oikopleura biomass is maximal in May. Oikopleura dioica, which has become a biological model to study these prochordates [FEN 86], was raised in the laboratory within a system that keeps the animals suspended without any contact with the container walls [FEN 79, LOM 09a]. Average generation time is nine days, but it is modulated by the temperature of water. Adults can produce from 4 to 16 houses per day [SAT 01]. Feeding rate strongly depends on temperature and food concentration [FEN 85, LOM 09a]. Particles larger than 30 µm are discarded

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by the primary house filter. Pico- and nanoparticles are concentrated on tangential filters inside the house. These animals are able to collect colloidal particles (transparent exopolymeric particles type). Water circulates in the house by pumping movements of the animal’s tail. The animal sucks the concentrate from tangential filters and aggregates it on its pharyngeal filter before ingestion. It has been shown that the animal can reject the concentrated particle if unfavorable cells are collected [LOM 11]. After digestion, the animal produces small and compact fecal pellets that are evacuated from the house by water circulation, or they stay in the abandoned house with clogged filters. Houses sediment slowly in the column of water, contributing to large aggregate formations that support bacterial and protistan communities. These aggregates become a food source for copepods and other predators that can locate the dissolved organic matter trail left by the aggregate [LOM 13]. Raising cohorts of Oikopleura dioica in the laboratory in order to measure growth (size of individuals and volume of gonads) and physiological variables gave the opportunity to design an individual-based model for this species [LOM 05, LOM 09a, LOM 09b]. From the model, some important physiological variables that are not directly accessible to measurement were estimated with the model, such as the minimum concentration of food to start feeding (20–30 µg C L−1) and the concentration for optimal growth (100 µg C L−1). The definition of an ecological niche for each appendicularian species allowed the authors to show their distribution in the world ocean [LOM 10]. A biogeochemical model including appendicularians was calibrated with the offshore conditions at the DYFAMED station [BER 11a]. Some theoretical estimations of vertical flux of matter compared to those observed in sediment traps at 200 m depth suggest that a large part of the detritus produced by appendicularians is degraded in the water column. Appendicularians are abundant in surface waters. However, some species such as Oikopleura villafrancae have been discovered in deep water [FEN 92]. The deep species Oikopleura villafrancae (1–10 individuals.m−3) living deeper than 300 m produce larger houses, 3–6 cm in diameter. It was observed, during dives with a manned submersible in offshore waters [LAV 89] and also using a video device (UVP: underwater video profiler) at different depths, in the range 430–620 m, depending on the distance from the shore. The abundance of small size particles, bacteria and other pico- and

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nanoparticles at these depths, depending on the slow downwelling flow of surface induced by the frontal dynamics along the North Current, was evidenced [GOR 91]. These appendicularians in their houses are easy prey for visual predators such as fish larvae (Pleuronectiforms, mackerels and congers) [PUR 05]. They appear as preferred prey for fish larvae and gelatinous carnivores [GOR 98]. Chordata (Phylum) Tunicata (Sub-Phylum) Appendicularia (Class) Copelata (Order) Fritillariacea (Fam.) Fritillaria Kowalevskiidae (Fam.) Kowalevskia Oikopleuridae (Fam.) Oikopleura Thaliacea (Class) Doliolida (Order) Doliolum Pyrosomatida (Order) Pyrosoma Salpida (Order) Salpa, Thalia Box 4.1. Taxonomic structure of pelagic tunicates (according to WoRMS, and reference to common genera from the Mediterranean Sea)

4.1.5.2. Thaliaceans (salps, doliolids, pyrosomids) Salps grow and proliferate in huge and sudden blooms, as a consequence of their complex lifecycle combining asexual and sexual stages, and their high feeding efficiency. As they can filter large volumes of water and retain small particles, even the smallest pico-size cells, they have the ability to influence the spring development of phytoplankton. The blooms of these animals have been recorded by Braconnot [BRA 63]. The interannual trends of abundances of Salpa and Thalia were described by Ménard et al. [MÉN 94]. The spatial scale of these blooms is not well documented in the Ligurian Sea. The lifecycle of these herbivores involves two different stages (Salpa fusiformis as an example). The egg develops into an individual called

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oozoïd, which produces by asexual budding, chains of colonial clones called blastozoïds. The male gonad maturing first, the female one appears in old individuals. Each female produces one oocyte that stays protected after fecundation in a special structure similar to a uterus, as well as an embryo. Spermatozoids shed in the water by young blastozoïds have to find their way to the oocytes. Each blastozoïd produces one oozoïd. At sea, the proportion of oozoïds in the population remains low [NIV 90]. An undisturbed animal slowly pumps water. A mucous net with a very fine mesh extends through this inhalant current along the gill to the mouth, collecting most of the pico-, nano- and microplankton cells [BON 91, DAD 19]. The net and packed particles are ingested and digested. Undigested matter is egested as flat and rectangular pellets that sediment rapidly to deep waters at a speed exceeding 500 m d−1 [YOO 96]. These individuals swim rapidly and filter several liters of seawater per hour. Isolated individuals or chains of individuals can swim forward or backward. Movement of blastozoïds in one chain is coordinated such that one chain can move backwards after contact with the leading individual [BON 98]. A careful study of swimming behavior and energetics of salps collected in Villefranche Bay has been published by Bone and Trueman [BON 83]. A nycthemeral migration of the species Salpa fusiformis has not been observed in the Ligurian Sea; however, an ontogenic migration could explain the sampling of a deep population of this species [SAR 96, YOO 95]. The maximal abundance of Salpa and Thalia in coastal waters can occur in a few days [BRA 71a]. High bloom densities show large amplitude variations that might suggest a high degree of patchiness of salp populations. Most of the year, salps remain at low density. Salpa fusiformis appears in surface plankton samples in Villefranche Bay at the end of December and can be abundant until surface temperature exceeds 15°C. The species Thalia democratica is present in spring and autumn. It is nearly absent or is at low density during summer [YOO 95]. Doliolids are small (few mm in length) and fragile animals with a high rate of asexual reproduction that produces blooms in the Ligurian Sea. Their

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complex lifecycle involving different life stages can explain these blooms [BRA 63, PAF 99]. The larvae, growing from an egg as an oozoïd, are able to produce buds of different types transferred onto a stolon. The number of phorozoids, each collecting a number of gonozoïds buds stored on the stolon, is progressively shed from the colony into the water. Male and female gametes are released in the seawater [BRA 71b, DEI 98]. As salps, they are micro-filters feeding on pico- and nanoparticles [CON 18]. The egg develops into a chordate larva that rapidly loses its tail and forms a typical doliolid shape [BRA 74]. Two species are known in the Mediterranean Sea, Doliolum nationalis, Borget, 1894 and Doliolina mülleri, Krohn, 1852. Their abundance is maximal during summer time in surface waters or late autumn [MÉN 97]. Pyrosomids are actually a colony of individuals. The impact of this type of large colony of microfeeders on phytoplankton is not well known. What is named a “pyrosome” is thousands of individuals (zooids) packed to form a tube closed at one end. These individuals pump water to collect food particles and eject the water inside the tube. The total flow of water produced by all the individuals exiting by the open end can produce a thrust and move the colony. A vertical migration up and down of these colonies has been observed [AND 92]. The zooids are possibly connected nervously to synchronize their activity, as salp blastozoïds are in their chain cluster. As the colonies increase in size, they are found at increasing depths during the day (6 mm long at 200 m and 25 mm at 600 m). Reproduction can either be asexual or sexual. Individuals in the colony produce buds giving new ones that stay close to their parent. This type of multiplication increases the size of the colony. Sexual reproduction produces an initial individual that soon reproduces asexually. The first colony of four zooids (tetrazoid stage) is frequently found in surface waters. All colonies migrate at night to the surface water where their phytoplankton food is abundant. Migration amplitude is 90 m for 3 mm-long colonies and 760 m for 51 mm-long ones. The mechanisms allowing the migration velocity estimated for largest individuals (150 m.h−1) are discussed by [BON 98]. The flux of fecal pellets was estimated in April 1991 in offshore waters of the Ligurian Sea, 28 nautical miles from Villefranche-sur-Mer, to 10 mg C m−2 d−1 with a pyrosomid biomass of 45 mg C m−2 [AND 94].

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4.1.6. Cnidarians All cnidarians are characterized by common morphological features: a radial symmetry plan, the absence of anus (the mouth serving both to feed and to expulse residues from digestion) and the presence of cnidocysts that are specialized cells containing a harpoon-like structure. Those cells react to mechanical signals and can evaginate their harpoon at unexpected speeds [TAR 95], delivering a cocktail of venoms to immobilize, kill or sometimes pre-digest the prey. Cnidaria (Phylum) Hydrozoa (Class) Hydroidolinae (sub-Class) Anthoathecata (Order) (Anthomedusae) Cladonema, Zanclea Leptothecata (Order) (Leptomedusae) Obelia, Clytia Siphonophorae (Order) Calycophorae (sub-Order) Chelophyes, Abylopsis Cystonectae (sub-Order) Physsophora Physonectae (sub-Order) Forskalia, Agalma Trachylinae (sub-Class) Actinulidae (Order) Limnomedusae (Order) Narcomedusae (Order) Solmissus, Solmundella Trachymedusae (Order) Aglaura, Liriope Scyphozoa (Class) Coronamedusae (sub-Class) Semaeostomeae (sub-Class) Pelagia Discomedusae (sub-Class) Rhizostoma Box 4.2. Taxonomic structure of cnidarians (according to WoRMS, and reference to common genera from the Mediterranean Sea)

4.1.6.1. Hydrozoa Hydrozoans are predators of micro- and mesozooplankton. Although they belong to the same taxonomic group, these animals exhibit different shapes [BOU 04]. The main differences in morphology lie between “medusa” and

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“siphonophora”. All small medusae have a similar aspect due to their bell shape, with a ring of tentacles and a mouth at the end of the clapper. However, a difference in the lifecycle (with or without a benthic stage) yields contrasting population dynamics. Overall, 65 species of small medusae have been observed in samples collected in surface water of the Bay of Villefranche-sur-Mer [GOY 68] and over three years in the 0–500 m column of coastal water offshore Villefranche-sur-Mer [GOY 16]. 4.1.6.1.1. Sub-class Hydroidolina (order Anthomedusae, Leptomedusae or Anthoathecata, Leptothecata, Siphonophores) Anthoathecata medusae (formerly Anthomedusae) are reproduction propagules produced by benthic nude hydrarians (athecate). Leptothecata medusae (formerly Leptomedusae) are the reproductive propagules produced by protected hydrarians (thecate). The role of these asexually produced free medusae is maturing sexual products. As they are transported by currents, they disperse the benthic species. Fertilization gives rise to larvae sinking soon to a benthic substrate. Although the benthic hydroid species from the genus Clytia are morphologically different, their medusae are very similar, so they appear in plankton records as Clytia spp. The same also applies to Obelia species. Clytia larvae can also attach to any hard-floating substrates like bits of wood and plastic pieces and can produce a polyp colony as the benthic stage of this animal. Because of their pelago-benthic lifecycle, most of the medusae from this group are found in coastal waters. They are ambush predators of mesozooplankton. Some medusae species are able to multiply asexually as benthic polyps do, bypassing the benthic stage [CAR 90]. Some species can develop as a pelagic polyp colony of the group of Anthoathecata. They were formally considered as Condrophores: Vellela and Porpita with repectively Chrysomitra and Discomitra medusae. These floating hydroid colonies shed medusae that ensure their reproduction. Velella can be concentrated by wind and be beached in large numbers on the coast, mostly between May–June. The ecology of these species is not well known in the Ligurian Sea. Siphonophores are considered to form an order in the sub-class Hydroidolina (WoRMS). They are important predators of meso-zooplankton, especially copepods. Three types of siphonophores can be encountered: physophore, cystonect and calycophore. The last one is the smallest and the most abundant, and has consequently received much more attention than the

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other two groups. Large physophores are colonies of polyps which have different morphologies and different roles (buoyancy, motion, feeding). Nevertheless, this colony behaves as a single animal, each polyp depending on the others through food channels and nervous connections. Polyps are distributed in the animal in three sections: – a single pneumatophore that ensures buoyancy of the colony, but might be absent; – a nectosome section with many polyps that have a swimming function; – a siphosome section grouping polyps in the role of collecting food. All the polyps are connected by a stolon that is the stem of the colony distributing food and by a nerve system to distribute information. New polyps are continuously produced by budding from defined sections of the colony. Gastrozoïd polyps are designed to digest the prey collected by tentacles equipped with stinging cnidocytes. Stolon and tentacles can be extended over a very large distance.

Figure 4.2. Examples of siphonophores recorded in situ in the frontal area of the Ligurian Sea. A: Lensia conoidea or Chelophyes appendiculate. B: Lilyopsis medusa (formerly L. rosea). Credit: images from the VISUFRONT cruise; PIs: J.-O. Irisson and R. K. Cowen, Funding: PUF RSMAS-OOV, Flotte Océanographique Française

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We can assume that, except when they are migrating or escaping when disturbed, the siphonophores rest, extending the stolon and tentacles in order to increase the fishing surface or volume. They should optimize the surface of tentacle netting with a curled movement [MAC 87]. Biggs et al. [BIG 87] estimated by blue SCUBA diving abundance of the large siphonophores in coastal waters of the Ligurian Sea to one animal per 6000 m3. Their presence in plankton net samples is only indicated by nectosome parts detached from the disintegrated colony when encountered during the plankton tow. Frequent species are Halistema, Physophora, Forkalia, Agalma and Apolemia. Cystonects: these siphonophores have a simple morphology. A very long stolon with bracts, tentacles and gastrozoïds hang as a long line under large pneumatophore, giving some buoyancy to the colony. Physalia has a very large pneumatophore that floats at the surface of the sea. Calycophores: most calycophore species are small-sized colonies of polyps. They are easily collected by plankton nets. They have no pneumatophores, but in most species, two swimming polyps (swimming bells), but Hippopodius hippopus has several, and some species have only one. Calycophores possess a long stolon with groups of gastrozoïds, tentacles and bracts, which can be deployed as a fishing line. When disturbed, the animal retracts the stolon in appropriate cavities of swimming bells. The terminal groups of polyps can detach from the stolon and transform to a reproductive stage (eudoxid) with new characteristics and budding of gonozoïds. This type of ambush predator swims rapidly on a curved trajectory to extend its stolon and rest, waiting for prey contact. Eudoxids exhibit the same behavior. These animals migrate from the crepuscular depth to the surface at night in order to reach a layer with abundant mesozooplanktonic prey. In escape mode, they can swim rapidly. They can perform large nychthemeral migrations. Their annual dynamics in the Bay of Villefranche was described by Buecher [BUE 99], and their long-term time variation was described by Licandro et al. [LIC 12]. 4.1.6.1.2. Trachylina (Trachymedusae and Narcomedusae) Although these medusae are similar in shape and size to Hydroidolina medusae, their lifecycles are very different. Having no benthic polyp stage, Trachymedusae and Narcomedusae can live in offshore waters. They are true

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planktonic species (holoplanktonic species) and ambush predators of mesozooplankton. Narcomedusae are usually found in deep waters. Their lifecycle is entirely pelagic. The large species Solmissus albescens, 4–5 cm in diameter, is common in the Ligurian Sea where it performs large nycthemeral migrations from 700 m depth to surface [AND 92, MIL 88]. The effect of medusae on copepods, in parallel with a change in the climatic forcing, was evident within the decadal-scale time series (1967–1994) in the Bay of Villefranche. This effect was interpreted as an increased control by gelatinous carnivores on the copepods after 1985, and suggests that top-down control on copepods in the macrobial food web might be as efficient as a bottom-up control of these crustaceans by their food resource. 4.1.6.2. Scyphozoa (Scyphomedusae) These medusae have morphological traits different from hydromedusae with the presence of a four-order symmetry visible on stomach pouches and oral arms. This group has two types of lifecycle, i.e. with and without a benthic phase. Species with a benthic polyp are found in coastal water mostly in spring (Rhizostoma pulmo) or late summer (Cotylorhiza tuberculata), and those without a benthic polyp are found all over the Ligurian Sea (Pelagia noctiluca). At least one species lives in deep water (Periphylla periphylla) at very low abundance. Other species such as Aurelia or Chrysaora can be found occasionally. Pelagia noctiluca, which has no benthic stage, is fully holoplanktonic. Its pelagic planula larva transforms directly into the juvenile “ephyra”, which progressively grows in size into the shape of the adult medusae. The release of gametes in the sea by aggregated adults produces large numbers of eggs that disperse [LIL 14a]. Generation time of this species is several months but it can survive for years, depending on the temperature and feeding conditions [LIL 14b]. At night, Pelagia migrates vertically from a parking depth in the mesopelagic zone to the surface [FRA 71] where it feeds during nighttime. As this medusae can be observed at the sea surface after sunset with the naked eye, monthly counts of adults per unit surface were carried out on a transect offshore Villefranche at different seasons. It has been shown that the observation frequency of Pelagia is higher during nights without moonlight, mostly in the frontal zone [FER 12].

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This species appears to develop preferentially in areas of high mesozooplankton biomass, especially in the frontal zone where larvae (ephyra) have been collected [MOR 92]. The prey of these medusae (mainly copepods) are more abundant in the frontal zone than in coastal waters [BOU 87, MOL 08a, MOL 08b]. However, the meandering of the North Current induces some transport and dispersion of Pelagia populations in coastal waters. During summer, it is common for cohorts of Pelagia to be pushed into coastal areas and stranded on beaches, generating strong psychosis in seashore vacationers. Records of the presence of large planktonic species in the Bay of Villefranche from 1898 to 1914 suggested that Pelagia was frequently observed during periods of 10 years. In these data, when they are absent for several years, the medusa Rhizostoma pulmo appears frequently [MOR 85]. However, in recent years, the two medusae have appeared simultaneously. Stranding records of this Pelagia species in published papers have been collected by Goy et al. [GOY 89] since the year 1800. These data suggest a 12-year periodicity of Pelagia blooms. Recent observations show a continuous occurrence since 1994, and now the proportion of tourists stung by Pelagia during summer has become a criterion for the stranding frequency [BER 11b]. The model of Berline et al. [BER 13], estimating the stranding and combining a population dynamics model to a hydrodynamic model simulating the flow of water along the north coast of the Ligurian Sea, suggested that medusae are transported from the frontal zone to coastal areas. 4.1.7. Ctenophores Ctenophores are transparent and extremely fragile animals and most of the species become pieces of gelatine when sampled by plankton nets. However, a small number of species are rigid enough to be collected properly. They are characterized by the presence of eight rows of hundreds of “ctenes” (combs), transparent paddles composed of thousands of ciliae glued together that reflect the light in prismatic colors. They swim thanks to pulsatile beating of these paddles. The lifecycle of some species is known from cultivation in the laboratory. Most feed on mesozooplankton. They secure their prey with sticky organs (colloblasts) distributed on tentacles. They are hermaphrodites, capable of releasing thousands of eggs every day.

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Although eggs are unfertilized when released, some level of self-fertilization might occur. The number of common species is small, and most of them appear to be epipelagic. However, some species have been discovered in deep water in the Ligurian Sea. The different groups of species have distinct anatomy and way of feeding: – Cyddipids: spherical and transparent, they catch prey with two long and branched tentacles covered with sticking elements (colloblasts). They extend their tentacles in order to collect prey by swimming on a curved trajectory. These ctenophores are not destroyed in plankton net tows. Pleurobrachia (sea gooseberries) is usually present in spring but has been less present since 2004. – Cestides: the surprising animal, Cestus which is the shape of a large and long ribbon, far from the more common spherical shape of ctenophores, occurs in the Ligurian Sea mostly during winter up to spring [MOR 85]. – Lobates: they usually loose or reduce their tentacles while growing from larvae to adult and develop important lobes from the four expansions of the pharynx, two of them forming large lobes in the shape of a sort of funnel similar to a plankton net. The animal swims slowly with its mouth facing forward and collects mesozooplankton prey by closing their lobes. A recurrent species is Leucothea multicornis, which occurs in late winter. Mnemiopsis leydii, which is a non-native species, an invader, is occasionally seen in the coastal Ligurian Sea since 2009, mostly in May. – Nuda: their aspect is a transparent flaccid cylinder equipped with the usual eight lines of paddles. They have no tentacles. They use their large pharynx and muscular mouth to engulf the prey they encounter on their slow swimming trajectory. Most of them are predators of other species of ctenophores. These fragile species, difficult to collect with plankton nets, probably migrate to the surface at night. The usual species is Beroe cucumis while some rare occurrence of Beroe formosa can be observed. Both occur during spring.

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Figure 4.3. Some macroplanktonic species from the Ligurian Sea. A. Siphonophore: Physophora hydrostatica (physophore); B. Ctenophore: Leucothea multicornis; C. Ctenophore: Beroe cucumis; D. Pelagic mollusk: Pterotrachea coronate; E. Thaliacean: Pyrosoma atlanticum; F. Thaliacean: Salpa maxima oozoïd. Underwater pictures (credit: David Luquet). For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

4.2. Micronekton 4.2.1. Euphausiids Euphausiids have a special status in the food web. They are a resource for cephalopods, whales and fish (tuna). They consume primary producers, but some species are probably detritus feeders and carnivores. The euphausiid community in the Ligurian Sea includes 15 species among which five are the most common and numerically dominant: Meganyctiphanes norvegica, Nematoscelis megalops, Euphausia krohnii, Stylocheiron longicorne and Nyctiphanes couchii – in order of decreasing importance.

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Regardless of the season, Meganyctiphanes norvegica is usually the most abundant in nearly all samples. Casanova [CAS 74] highlighted the significance of this species in the northern part of the Western Mediterranean, which is the coldest part of the Mediterranean, and described the frequency variation of individuals off Villefranche. Euphausia krohnii is more frequent at the end of summer and autumn, whereas Stylocheiron longicorne is frequent all year. Nematoscelis megalops is the second largest species in quantity, more frequent in spring and summer [CAS 74]. During summer and autumn, Meganyctiphanes norvegica concentrates at night in surface waters close to the coast during the reproduction period. Labat and Cuzin-Roudy [LAB 96] described the population dynamics in the Ligurian Sea from Isaac Kid net fishing (day 700–0 m and night 100–0 m). Other species such as Nyctiphanes couchii can concentrate in dense patches. The lifecycle of these species involves several stages in surface waters. The biomass of euphausiids is high. Some species are herbivorous and produce cylindrical fecal pellets that represent a large downward flux and are one of the most important items in sediment traps. Meganyctiphanes norvegica, named “krill” by Norweigian fishermen, is present in the North Atlantic along the European west coast, from Greenland to the North Sea, down to the Bay of Biscay, Portugal, the Bay of Cadiz, Cape Verde islands and west Morocco, down to Cape Juby [THI 77] – all coasts with active upwelling. Krill is a keystone species in the Mediterranean trophic webs, being prey of pelagic as well as deep benthic predators (e.g. tunas, mackerels, dogfishes, hake, blue whiting, sharks, cetaceans and birds). In particular it is essential for the survival of the fin whale, Balaenoptera physalus (see Chapter 5). The Ligurian krill becomes mature the second year of its lifecycle at 32–33 mm total body length, and releases eggs in successive spawns during spring (February–May), when the offshore cold surface water indicates strong deep mixing leading to the spring bloom of phytoplankton, and next zooplankton, which the seasonal abundance of the omnivorous M. norvegica depends upon. Gonadal activity and growth stop, or are even reversed, as adults return to a juvenile size during summer and autumn. The entire winter cohort of juveniles (from year 1 and year 2) will become adults during spring of the next year [LAB 96]. In summer, krill have a patchy distribution with the main concentration found in the Liguro-Provençal Front – the foraging area for fin whales.

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M. norvegica swims permanently and has a swarming strategy to mislead predators [SIM 10]. In the Ligurian basin, the main part of the krill population performs night vertical migrations from the deep water (−400 m) to the superficial zone (0–100 m) to feed on phyto- and zooplankton (mainly diatoms and copepods). M. norvegica avoids light, even moonlight, and only comes to surface water during nights without moonlight (dark clouds, new moon, lunar eclipse, etc.) and returns to depth early at dawn [TAR 99]. Molting and mating krill aggregates on the shelves or sea bottom and stays there over one or two days to consolidate their new cuticle and to forage the sediment for prey whilst avoiding predators [CUZ 10, TAR 03]. The genetic make-up of seven populations of M. norvegica from different regions of the North Atlantic and Mediterranean Sea (Kattegat, Skagerrak, Clyde Sea, Rockall Trough, Alboran Sea, Ligurian Sea and Bay of Cadiz) were studied. Three distinct genetic pools were revealed: the first represented the Cadiz Bay krill, the second one the Ligurian Sea krill, and the third one the North East Atlantic krill. The population from the Alboran Sea (east of the Strait of Gibraltar) was added and was found to be genetically intermediate between the North Atlantic sample and the Ligurian sample, suggesting that the restriction to the gene flow is not associated with the Strait of Gibraltar, but possibly with the Oran-Almeria oceanographic front [ZAN 00]. These results indicate that M. norvegica sp. can develop separate breeding units inside the same oceanic basin, the North Atlantic (East and West). The Mediterranean krill can be considered as a distinct evolutionary entity, separated from the Atlantic krill population. M. norvegica may be influenced by the ongoing temperature elevation in warm and dry summers. The response of the Mediterranean krill avoiding full light, staying in cold deep water, down to -2000 m depth in the Ligurian Sea, is a positive strategy, as the most vital krill traits are preserved: feeding, growth and molting, mating and reproducing [CUZ 99a, CUZ 99b]. In contrast, the Mediterranean krill population adaptive strategies may have attained their limits, facing the rapid climate change of the Mediterranean Sea and other impacts such as the invasions by tropical species coming through the open Suez Canal, habitat loss and degradation due to human activities along the coasts, as well as in the pelagic realm (i.e. increasing input of nutrients and anthropogenic carbon). The Ligurian Sea is an area of important primary production that sustains a relatively high production of zooplankton biomass. Here, many top pelagic

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predators concentrate, some foraging exclusively on M. norvegica (e.g. fin whale, young bluefin tuna), others exploiting its abundance as seasonal main prey. Obviously, alterations of the oceanographic processes due to the higher temperature of the water masses, as happened during the summers of 2016 and 2017, or increased temperature during the first months of the year, may affect the dynamics of the krill population, which reverberates onto the feeding and reproductive behavior of its predators, as well as the phyto- and zooplankton (e.g. diatoms, copepods) abundance on the krill itself (bottomup control). In spite of the krill’s ability to adapt its reproductive cycle to different habitats by using the flexibility of the physiological cycles involved in gonad development (a strategy that allows enhancing fecundity and to tune the reproductive effort with food availability for the offspring [CUZ 93]) a possible scenario, due to an increasing water temperature of the Ligurian Sea, can be drawn considering the spatial and seasonal shift of the presence and distribution of its predators, already in place in this area. 4.2.2. Other micronekton species Large marine species are usually considered to be at the top of the food web, many of them being carnivorous predators. These top predators, including fish, mammals and also large mollusks such as squid (see Chapter 5), swim quickly and move in a very large area without being influenced by currents. They are elements of the Nekton. Many migrate long distances between feeding, breeding or even wintering zones, unlike macroplankton animals that are passively transported by currents. Estimating their abundance requires special tools (pelagic trawls, acoustic, visual enumeration). Smaller species (micronekton) that swim quickly are caught in the nets used to harvest macroplankton (small pelagic trawls or plankton nets with large openings, 1 to several m2). These sampling tools can be used to estimate the abundance of micronekton species. Collected in the same samples as macroplanktonic animals, they are studied together. Micronekton animals, i.e. fish, crustaceans or cephalopods, as observed from manned submersibles, often show the immobility of a species in ambush. However, their belonging to the micronekton type comes from their ability to escape quickly, and over a long distance, when disturbed. Few studies on micronekton have been conducted in the Ligurian Sea or the North West Mediterranean Sea [FRA 71, PAL 90, SAR 96, VUD 78].

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The annual variation and vertical distribution of adult abundance are documented, while those of larvae and juveniles are often ignored. The larvae and juvenile are small in size, and the identification of developmental stages is difficult, especially because these pelagic species have numerous different stages during their development. Sardou et al. [SAR 96] and Franqueville [FRA 71] studied vertical distribution and annual cycles of abundance, respectively off Nice and south of Marseille with the IKMT (Isaac Kid Midwater Trawl). A tentative list of species that are regularly caught can thus be established. Mesopelagic fish Cyclothone braueri, Cyclothone pygmea, Argyropelecus hemigymnus. Andersen and Sardou [AND 92], measuring day and night abundance profiles with a BIONESS net, showed that Argyropelecus migrates in the Ligurian Sea from 410 m to 260 m, while the two Cyclothone species do not migrate (C. braueri at 500 m, C. pygmea at 700 m). In addition, the profiles obtained on a Nice–Calvi line suggest a deepening of C. braueri at their stationary depth, in the center of the transect [AND 98]. Crustaceans Euphausiids: Meganyctiphanes Nematoscelis megalops.

norvegica,

Euphausia

krohnii,

Decapods: Pasiphaea sivado, Sergestes arcticus, Acanthephyra pelágica. Annual cycle and vertical distributions were found by Franqueville [FRA 71] and Sardou et al. [SAR 96]. In the literature concerning the Ligurian Sea, euphausiids have received more attention than decapods. Cephalopods A few small species live in open water where their presence is generally noted. Sometimes a cephalopod larva is found in a sample from a plankton net. There is a lack of information on these species. Except for euphausiids, which can capture microphytoplankton, other species are predators of mesozooplankton. Sergestes eximia and Cyclothone

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pygmaea are considered as endemic species in the Mediterranean Sea [SUT 17]. The scattered data on the presence or abundance of these animals make it difficult to assess the mortality they induce on zooplankton. It is also difficult to estimate the amount of nutritional resources these micronekton species represent for macronekton species (fish, whales and their large prey, squid). 4.3. Zooplankton long-term series 4.3.1. Introduction In marine ecosystems, changes in the structure and composition of the plankton communities have been observed and related to temporal variation in hydro-climatic variables [BEA 02, BEA 03, BEA 04, EDW 02, LEH 06]. Temporal fluctuation in the plankton community structure affects ecosystem services such as tourism by jellyfish proliferation or industrial activities such as fisheries as fish larvae forage on plankton.

Figure 4.4. Sites in the Northern Hemisphere where zooplankton has been collected and the datasets archived in the Coastal and Oceanic Plankton Ecology, Production and Observation Database (COPEPOD). The Observation station in the Bay of Villefranche, named Point B (white circle), shown on this map. Apart from the Continuous Plankton Recorder survey since 1933 in the Northern ocean (grid pattern), Point B (white circle) time series is the longest and most complete in European waters (from [OBR 13]). For a color version of this figure, see www.iste.co.uk/migon/mediterranean2.zip

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It has been proposed that plankton is a good indicator of climate change for several reasons. Most species are not being commercially exploited and the long-term changes observed in their stocks can therefore be attributed to changes in environmental conditions. As organisms living in suspension in the water column, they are good indicators of the features and dynamics of water masses. In addition, they have a short lifespan that facilitates relating population size to environmental conditions. Finally, plankton, with their nonlinear responses to environmental changes, can amplify subtle environmental perturbations that otherwise would not be perceived [TAY 02]. Time series of biological and environmental parameters represent a unique and very important tool in the understanding of the relationship between environmental forcing and plankton dynamics. Therefore, in an era of severe change in the forcing on marine systems, initiatives to monitor marine coastal and open ocean plankton have increased in the last decades [WGE 13, LAR 15]. In Europe, the Marine Strategy Framework Directive (MSFD: 2008/56/EC) considers the marine systems through an ecosystem approach, and plankton is one target of this program. Despite the recognized importance of monitoring plankton, there are very few long-term (a few decades) observation sites, globally (see https://www.st.nmfs.noaa.gov/copepod/, Figure 4.4), and in particular in the Mediterranean Sea (six long time series [BER 12]). 4.3.2. Zooplankton temporal trends in the Bay of Villefranchesur-Mer as an indicator of Ligurian Sea dynamics The longest Mediterranean zooplankton time series is the one conducted since 1966, without interruption, at Point B in the Bay of Villefranche (Ligurian Sea). Plankton is collected everyday using three different nets of different mesh size (WP2 net with 200 µm, Juday-Bogorov net with 300 µm, Regent net with 680 µm). More than 25 publications have been produced over 53 years with a progression in the knowledge on plankton temporal dynamics from seasonal to interannual scales. With longer time series, the possibility to disentangle interannual scales linked to climatic variability such as the North Atlantic Oscillation (NAO) and long-term warming has been appraised by the researchers in the marine station of Villefranche-surMer. Only recently, inter-comparisons between zooplankton time series

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obtained globally have allowed us to understand global synchronicity of changes and their overall driver: the increase in temperature.

1985

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The first 20 years after the establishment of the standardized zooplankton sampling, the time-series data could only be used to describe the plankton community [SEG 81], to depict seasonal cycle of plankton [BOU 68, NIV 75a, NIV 75b] or to develop statistical methods coping with predictable future large datasets [IBA 69, IBA 81, IBA 82, IBA 84]. In the 1980s and early 1990s, after 20 years of observation, the first results on the decadal oscillation of plankton were published [BRA 90, GOY 89, MÉN 94, MOR 85] in attempts to understand the massive periodic proliferation of the Pelagia jellyfish (Figure 4.5).

Figure 4.5. Pelagia noctiluca time series. Proliferation years were associated with high rain in Genoa airport (from [GOY 89])

In the 1990s, zooplankton collection continued but taxonomy experts vanished as retiring scientists were not replaced by a new generation. For an unknown reason, jellyfish proliferation also decreased in the 1990s without any explanation apart from the finding that years without massive proliferation corresponded to high winter rainfall recorded at the airport of Genoa (Italy). In addition, the fashion in oceanographic research had moved to biogeochemistry to quantify mass flux in the ocean, ignoring the organisms.

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However, in the middle of the 1990s, some young scientists worked again on target species easily identified in the multitudes of samples such as the copepod Centropages typicus or the medusae Liriope tetraphylla and Pelagia noctiluca. Buecher et al. [BUE 97] showed that the interannual cycle of the two jellyfishes were synchronized with changes in winter forcings, identifying dry years (with low cloud coverage and rain in winter) and wet years. Molinero et al. [MOL 05a, MOL 05b] studied the abundance of several copepod, jellyfish and siphonophore target species from 1967 to 1993 at Point B. For the first time after 40 years of sampling, the authors proposed a cascade of links between the large-scale climate pattern occurring in the North Atlantic, and the local climate variability governing the north-western Mediterranean. The sequence of events appeared to be driven by the long-term temperature anomalies that in turn played a key role in the top-down control of copepods by jellyfish. Further research on the same long-term pelagic time series, with chaetognath temporal evolution, included in the analyses, suggested that a regime shift had taken place in 1987 in the Ligurian Sea [MOL 08a]. According to the authors, the system evolved towards a more regeneration-dominated ecosystem in which copepods were controlled by jellyfishes and chaetognaths by predation and competition, respectively. Thermal stratification was appointed to be the main force ruling zooplankton composition, and a community dominated by gelatinous zooplankton was hypothesized for the Ligurian Sea [MOL 08a]. However, due to the lack of permanent technical skills and recruitment of scientists, samples ceased to be analyzed and it was not possible to verify the hypothesis nor to verify whether those changes would affect the whole plankton community. Fortunately, the recruitment of scientists and technical staff in the 2000s at the marine station allowed analysis of the whole time series of the JudayBogorov (1966–2003) and WP2 nets (1995–2006) with the new ZooScan imaging systems [GOR 10]. Results showed that the abundance of the jellyfish community did not increase from the late 1980s despite thermal increase [GAR 11, VAN 11] (see Figure 4.6). In addition, all the studied groups showed anomalies of the same sign between the 1980s and the 1990s, which suggests that they might be mainly subjected to bottom-up control. Both studies also showed that a second shift in the plankton community was observed after the 2000s.

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Figure 4.6. Left: weekly time series of total zooplankton abundance. Black stars correspond to original measurements without treatment. The red curve corresponds to the smoothed time series. The magenta stairs correspond to the STARS shifts detection method [ROD 06] which detects significant changes in the mean. Here, a significant increase (α = 0.05) by 1.84 is recorded in February 2000. Right: median of weekly values of total zooplankton during wet years before 2000 (black) and after, during dry years (red) with percentiles Q1 and Q3 (shaded area), from [VAN 11]. Middle: annual cycles of modeled zooplankton colored according to the annual value of MLD index (blue for low MLD during wet years, red for high MLD during dry years) (from [AUG 14]). For a color version of this figure, see www.iste.co.uk/migon/ mediterranean2.zip

The authors confirmed the climate cascade but proposed the winter physical forcing on primary production as the most significant factor driving the changes in the annual standing stocks of copepods, chaetognaths, decapod larvae, siphonophores and jellyfish. They hypothesized that interannual fluctuations in winter in the North Atlantic is the main driver of plankton dynamics despite increasing evidence that long-term trends in global warming may have consequences in summer community composition. Recent biogeochemical modeling has confirmed the two states of the plankton community as forced by winter mixing [AUG 14] (see Figure 4.6, right). During dry years, deeper MLD triggers a high load of nutrients in the surface layer and, thus, primary production beneficial for zooplankton. In contrast, during wet years, less nutrients are mixed in the surface layer to the

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detriment of the plankton trophic web. The impact of these interannual changes in plankton ecology has consequences for the carbon sequestration in the deep waters [AUG 14]. 4.3.3. From local variability in plankton to global understanding and plankton community forecasts The recent appearance of regime shifts with their turning points in 1987 in two northern Mediterranean coastal ecosystems (Ligurian and Adriatic Seas) and their synchrony with changes in the Atlantic Ocean and the Baltic and Black Seas has been highlighted [CON 10]. In all cases, the authors pointed to the positive trend of surface temperature in the Northern Hemisphere as the main forcing for the concomitant changes in such far and diverse locations. To confirm synchronized shifts in the plankton community, the Point B time series was combined with 11 marine systems from two oceans and three regional seas in the Northern Hemisphere in a more formal statistical analysis [BEA 15]. Results showed that the main shift at the end of the 1980s was observed in all of them while some also exhibited secondary shifts. The results suggested that the main factor synchronizing regime shifts on large scales is the Northern Hemisphere temperature; however, changes in atmospheric circulation also appear to be important. Finally, combining Point B time series with 13 other marine biological systems and a global numerical model based on a niche theory forced by temperature, a recent work predicted global shifts in the biological community in the ocean and assessed the spatial extent of those shifts [BEA 19]. Finally, this work alerts us about the potential for an increase in the size and consequences of such shifts in the future as the world warms in response to global climate change. 4.4. References [AND 92] ANDERSEN V., SARDOU J., NIVAL P., “The diel migrations and vertical distributions of zooplankton and micronekton in the northwestern Mediterranean Sea. 2. Siphonophores, hydromedusae and pyrosomids”, Journal of Plankton Research, vol. 14, pp. 1155–1169, 1992. [AND 94] ANDERSEN V., SARDOU J., “Pyrosoma atlanticum (Tunicata, Thaliacea). Diel migration and vertical distribution as a function of colony size”, Journal of Plankton Research, vol. 16, pp. 337–349, 1994.

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[AND 98] ANDERSEN V., FRANÇOIS F., SARDOU J. et al., “Vertical distributions of macroplankton and micronekton in the Ligurian and Tyrrhenian seas (northwestern Mediterranean)”, Oceanologica Acta, vol. 21, pp. 655–676, 1998. [AUG 14] AUGER P.A., ULSES C., ESTOURNEL C. et al., “Interannual control of plankton communities by deep winter mixing and prey/predator interactions in the NW Mediterranean: Results from a 30-year 3D modeling study”, Progress In Oceanography, vol. 124, pp. 12–27, 2014. [BEA 02] BEAUGRAND G., REID P.C., IBANEZ F. et al., “Reorganization of North Atlantic marine copepod biodiversity and climate”, Science, vol. 296, pp. 1692–1694, 2002. [BEA 03] BEAUGRAND G., BRANDER K.M., LINDLEY J.A. et al., “Plankton effect on cod recruitment in the North Sea”, Nature, vol. 426, pp. 661–664, 2003. [BEA 04] BEAUGRAND G., IBANEZ F., “Monitoring marine plankton ecosystems. II: Long-term changes in North Sea calanoid copepods in relation to hydro-climatic variability”, Marine Ecology – Progress Series, vol. 284, pp. 35–47, 2004. [BEA 15] BEAUGRAND G., CONVERSI A., CHIBA S. et al., “Synchronous marine pelagic regime shifts in the Northern Hemisphere”, Philosophical Transactions of the Royal Society B – Biological Sciences, vol. 370, doi: 20130272, 2015. [BEA 19] BEAUGRAND G., CONVERSI A., ATKINSON A. et al., “Prediction of unprecedented biological shifts in the global ocean”, Nature Climate Change, vol. 9, pp. 237–243, 2019. [BER 11a] BERLINE L., STEMMANN L., VICHI M. et al., “Impact of appendicularians on detritus and export fluxes: A model approach at DyFAMed site”, Journal of Plankton Research, vol. 33, pp. 855–872, 2011. [BER 11b] BERNARD P., BERLINE L., GORSKY G., “Long-term (1981–2008) monitoring of the jellyfish Pelagia noctiluca (Cnidaria, Scyphozoa) on the French Mediterranean Coasts”, Journal of Oceanography, Research and Data, vol. 4, 2011. [BER 12] BERLINE L., SIOKOU-FRANGOU L., MARASOVIC I. et al., “Intercomparison of six Mediterranean zooplankton time series”, Progress In Oceanography, vol. 97, pp. 76–91, 2012. [BER 13] BERLINE L., ZAKARDJIAN B., MOLCARD A. et al., “Modeling jellyfish Pelagia noctiluca transport and stranding in the Ligurian Sea”, Marine Pollution Bulletin, vol. 70, pp. 90–99, 2013. [BIE 89] BIEKART J.W., “Euthecosomatous pteropods as paleohydrological and paleoecological indicators in a Tyrrhenian deep-sea core”, Palaeogeography, Palaeoclimatology, Palaeoecology, vol. 71, pp. 205–224, 1989.

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[BIG 87] BIGGS D.C., LAVAL P., BRACONNOT J.-C. et al., “In situ observations of Mediterranean zooplankton by SCUBA and bathyscaphe in the Ligurian Sea in April 1986”, Diving for Science…1986. Proceedings of the American Academy of Underwater Science. 6th Annual Scientific Diving Symposium, Tallahasse, FL, AAUS, 1987. [BON 83] BONE Q., TRUEMAN E.R., “Jet propulsion in salps (Tunicata: Thaliacea)”, Journal of Zoology, vol. 201, pp. 481–506, 1983. [BON 91] BONE Q., BRACONNOT J.C., RYAN K.P., “On the pharyngeal feeding filter of the salp Pegea confoederata (Tunicata: Thaliacea)”, Acta Zoologica, vol. 72, pp. 55–60, 1991. [BON 98] BONE Q., “Locomotion, locomotor muscles, and buoyancy”, The Biology of Pelagic Tunicates, Oxford University Press, Oxford, 1998. [BOU 68] BOUGIS P., NIVAL P., NIVAL S., “Distribution quantitative comparée du phytoplankton et des copépodes dans les eaux superficielles de la rade de Villefranche”, Journal of Experimental Marine Biology and Ecology, vol. 2, pp. 239–251, 1968. [BOU 87] BOUCHER J., IBANEZ F., PRIEUR L., “Daily and seasonal variations in the spatial distribution of zooplankton populations in relation to the physical structure in the Ligurian Sea Front”, Journal of Marine Research, vol. 45, pp. 133–173, 1987. [BOU 04] BOUILLON J., MEDEL M.D., PAGES F. et al., “Fauna of the Mediterranean Hydrozoa”, Scientia Marina, vol. 68, pp. 5–449, 2004. [BRA 63] BRACONNOT J.C., “Etude du cycle annuel des salpes et dolioles en rade de Villefranche-sur-Mer”, Journal du Conseil, CIESM, vol. 28, pp. 21–38, 1963. [BRA 71a] BRACONNOT J.C., “Contribution à l’étude biologique et écologique des tuniciers pélagiques salpides et doliolides. I. Hydrologie et écologie des salpides”, Vie et Milieu, vol. 22, pp. 257–286, 1971. [BRA 71b] BRACONNOT J.C., “Contribution à l’étude biologique et écologique des tuniciers pélagiques salpides et doliolides II – hydrologie et écologie des Doliolides”, Vie et Milieu, vol. 22, pp. 437–467, 1971. [BRA 74] BRACONNOT J.C., “Le tunicier pélagique Pyrosoma atlanticum Peron, 1804, en mer Ligure (Méditerranée occidentale)”, Rapports et Procès Verbaux de la Commission Internationale pour l’Exploration de la Mer Méditerranée, vol. 22, pp. 97–99, 1974. [BRA 90] BRACONNOT J.C., ETIENNE M., MOITIE M., “Distribution du tunicier pélagique Salpa fusiformis Cuvier à Villefranche : 13 années d’observations”, Rapp. Comm. int. mer Médit., vol. 32, p. 225, 1990.

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[BUE 97] BUECHER E., GOY J., PLANQUE B. et al., “Long-term fluctuations of Liriope tetraphylla in Villefranche bay between 1966 and 1993 compared to Pelagia noctiluca populations”, Oceanologica Acta, vol. 20, pp. 145–157, 1997. [BUE 99] BUECHER E., “Appearance of Chelophyes appendiculata and Abylopsis tetragona (Cnidaria, Siphonophora) in the Bay of Villefranche, northwestern Mediterranean”, Journal of Sea Research, vol. 41, pp. 295–307, 1999. [CAR 90] CARRÉ C., CARRÉ C., “Complex reproductive cycle in Eucheilota paradoxica (Hydrozoa: Leptomedusae): Medusae, polyps and frustules produced from medusa stage”, Marine Biology, vol. 104, pp. 303–310, 1990. [CAS 74] CASANOVA B., Les Euphausiacées de Méditerranée, Thesis, University of Provence, 1974. [CON 10] CONVERSI A., UMANI S.F., PELUSO T. et al., “The Mediterranean Sea regime shift at the end of the 1980s, and intriguing parallelisms with other European basins”, Plos ONE, vol. 5, p. e10633, 2010. [CON 18] CONLEY K.R., LOMBARD F., SUTHERLAND K.R., “Mammoth grazers on the ocean’s minuteness: a review of selective feeding using mucous meshes”, Proceedings of the Royal Society B: Biological Sciences, 2018. [CUZ 93] CUZIN-ROUDY J., “Reproductive stategies of the Mediterranean krill, Meganyctiphanes-norvegica and the Atarctic Krill, Euphausia-superba (Crustacea, Euphausacia)”, Invertebrate Reproduction & Development, vol. 23, pp. 105–114, 1993. [CUZ 99a] CUZIN-ROUDY J., ALBESSARD E., VIRTUE P. et al., “The scheduling of spawning with the moult cycle in Northern krill (Crustacea: Euphausiacea): A strategy for allocating lipids to reproduction”, Invertebrate Reproduction & Development, vol. 36, pp. 163–170, 1999. [CUZ 99b] CUZIN-ROUDY J., BUCHHOLZ F., “Ovarian development and spawning in relation to the moult cycle in Northern krill, Meganyctiphanes norvegica (Crustacea: Euphausiacea), along a climatic gradient”, Marine Biology, vol. 133, pp. 267–281, 1999. [CUZ 10] CUZIN-ROUDY J., “Reproduction in northern krill (Meganyctiphnes norvegica Sars)”, in G.A. TARLING (ed.), Advances in Marine Biology, vol. 57, Elsevier Academic Press Inc, San Diego, 2010. [DAD 19] DADON-PILOSOF A., LOMBARD F., GENIN A. et al., “Prey taxonomy rather than size determines salp diets”, Limnology and Oceanography, vol. 0, 2019. [DAL 68] DALLOT S., “Observations préliminaires sur la reproduction en élevage du Chaetognathe planctonique Sagitta setosa Müller”, Rapport Commission Internationale Mer Méditerranée, vol. 19, pp. 521–523, 1968.

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5 Climate Change Effects on the Ligurian Sea Pelagic Ecosystem. What About Top Pelagic Predators?1

5.1. Introduction The Mediterranean Sea can be described as a “miniature ocean”. However, because of its relatively small size and oligotrophy, along with high levels of biodiversity and endemism, and the fact that many oceanographic processes occur with a turnover time of about one-tenth of the global ocean, it has been predicted that the impact of climate change will be large and rapid. Indeed, data indicate significant warming of annual average temperatures both of the sea surface and water column. Future changes in climate-driven patterns of the thermohaline circulation could affect the Mediterranean ecosystem functioning as a whole, including deep-water habitats [CAL 11, KNI 15, LEJ 10, MAC 13, RIX 05, SCH 16]. The future scenarios indicate an experience of significant warming, peaking at more than 2°C per century [SHA 14] and extreme sea conditions may cause an increase of phenomena already underway, such as disease outbreaks among marine organisms [COM 09, DAN 09, LEJ 10], the spread of non-native species [AZZ 11, COL 10, EVA 15, BEN 09, RAI 10] and the shifting distribution of native Mediterranean fauna [ALB 12, AZZ 11, KNI 15, PSO 11]. Chapter written by Maurizio WÜRTZ and Jean-Marc FROMENTIN. The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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On the contrary, the Mediterranean Sea is also a complex marine ecosystem where variability of the oceanographic and biological processes is the rule, and the Ligurian Sea, the northernmost sector of the Western Mediterranean, is no exception. The variability of processes affects the distribution, abundance and behavior of many, if not all, top pelagic predators, both permanent residents and transient species using the area for feeding and reproduction. In this review, we attempt to summarize current knowledge on the possible impact of climate change on the top pelagic predators, focusing on the Ligurian Sea as a functional part of the Mediterranean ecosystem and addressing some key questions [MAU 05]: – What do we know about the species’ presence in the area, their reproductive and feeding behavior and how does the species’ presence and behavior vary in relation to climate variability? – What is the relative importance of mesopelagic and epipelagic prey resources of top pelagic predators and how does climate variability affect the distribution and availability of prey? 5.2. Top pelagic predators in the Ligurian Sea. What about species and what we know about their responses to local climate change? The terms “top pelagic predators”, referring to their position within the pelagic trophic webs, or “large pelagic predators”, referring to their size as pelagic animals, include a heterogeneous group of species living in the open sea from the surface to the deeper waters – squids, bony fishes, sharks, sea turtles, marine mammals and sea birds. They are often highly migratory and exert a strong top-down control over the population of their prey, and consequently play a key role in the functioning of the entire pelagic ecosystem. In addition, some of these species (i.e. Cetaceans) are considered a sentinel or indicator for the state of marine ecosystems, as well as umbrella species, which have special conservation importance [PAC 15]. In spite of this ecological importance, our knowledge about their biology and lifecycle is still incomplete, even about those species that have commercial importance. Through information from various publications

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with diverse audiences (taxonomy, fishery biology, genetics, abundance assessment, distribution, conservation, etc.) and new observation systems (e.g. electronic tagging, aerial surveys), it is possible to fill in some parts of the puzzle about possible effects on climate change on the populations of the top or “large” pelagic predators. 5.2.1. Squids Evolution has driven squids towards life in the “fast line”; they have high growth rates as well as continuous growth, efficient use of oxygen, fast metabolism, voracious appetite and efficient digestion, all designed for a short lifespan (about one year or less). Therefore, temperature increases can have complex effects on squids: shorter embryonic phase; faster growth and also high variance of growth rates; smaller adult size, thus earlier maturity and lower reproduction output, as well as shorter lifespan with temporal synchronicity of spawning activities reduced; higher recruitment variability also means alteration of annual biomass production, which is usually a cyclical phenomenon in Cephalopods [PEC 06]. Cephalopods are known to have rapid response times to climate change perturbations (both as population sensitiveness and resilience). It may therefore be difficult to distinguish between the effects of directional climate change and local climate variation, and in the case for all exploited species between these effects and the effects of fishing [PIE 10]. Most of the mesopelagic squids play a double role of both predator and prey. The largest squid (total length 170 cm, 86 kg weight) recorded in the Ligurian Sea belongs to the family Cranchiidae, genus Megalocranchia [BEL 99] (Figure 5.1 (left)). This specimen has been caught by a long line for blackspot seabream (Pagellus bogaraveo), similarly, the presence of other large mesopelagic squids in the area, known thanks to occasional bycatches of various fishing gears (e.g. Ommastrephes bartramii) or recreational jig fishing (e.g. Todarodes sagittatus), both species belonging to the Ommastrephidae family. In general, as a consequence of their low frequency in the fishery catches, the mesopelagic squid abundance is believed low. Nevertheless, a quite different picture can be deduced from hundreds of their beaks found in the stomach of top pelagic predators, such as dolphins, sharks or bluefin tuna.

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This is the case for Histioteuthids (Histioteuthis bonnellii and Histioteuthis reversa) (Figure 5.1 (Right) and 5.2 (Left)), Octopoteuthids (Octopoteuthis sicula) (Figure 5.2 (Right)) and Ommastrephids (Todarodes sagittatus, Ommastrephes bartramii, Illex coindetii, Todaropsis eblanae). Their biomass is likely to be much more important than previously estimated and, as they are also prey, even larger than the standing biomass of their predators (e.g. teuthophagous cetaceans); Histioteuthids, in particular, because their key role in the trophic webs of the Ligurian Sea, is being prey for many odontocetes, tuna, swordfish and sharks that exploit this part of the Mediterranean as a feeding area [ORS 95, WÜR 92, WÜR 93].

Figure 5.1. Mesopelagic squids. Left: Megalocranchia sp., mantle length (ML) up to 180 cm. Right: Histioteuthis bonnellii, ML up to 35 cm* (drawings by M. WürtzArtescienza). *Specimen found dead at the surface by one of the authors in the Ligurian Sea, on June 1995 at 43°02’.00N–7°57’.75E

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Figure 5.2. Mesopelagic squids. Left: Histioteuthis reversa, ML up to 20 cm. Right: Octopoteuthis sicula (reconstruction of an adult individual), ML possibly up to 50 cm (drawings by M. Würtz-Artescienza)

The Ommastrephid squid Todarodes sagittatus shows significant correlations between hatching success and temperature [QUE 04]. Mediterranean squids have wider embryonic increments in their statoliths than Atlantic squids [VIL 03] and a superior growth performance in the early life stages has been observed in ommastrephid species (broad-tailed shortfin squid Illex coindetii) hatched in warm conditions, compared to specimens hatched in colder conditions [PIE 08, RAG 02].

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In the Western Mediterranean, a general increasing trend in the abundance of the broad-tailed shortfin squid has been observed (which agrees with the already reported worldwide proliferation of cephalopods) and areas of high sea surface temperature showed higher densities of squid [KEL 17]. 5.2.2. Bony fishes 5.2.2.1. Bluefin tuna Atlantic bluefin tuna (Thunnus thynnus) (BFT) mainly lives in the temperate waters of the pelagic ecosystem of the North Atlantic and the Mediterranean Sea [FRO 05], but it can tolerate cold as well as warm temperatures while maintaining a stable internal body temperature. BFT preferentially occupies the surface and subsurface waters of the coastal and open-sea areas, but it can dive to depths of 500 m–1,000 m. It is also a highly migratory species, displaying a homing behavior and spawning site fidelity in both the Mediterranean Sea and Gulf of Mexico, which constitute the two main spawning areas clearly identified today [BLO 05]. The appearance and disappearance of important past fisheries further suggest that significant changes in the spatial dynamics of BFT may also have resulted from interactions between biological factors, environmental variations and fishing [FRO 09]. Although the BFT population is managed as two stocks, conventionally separated by the 45°W meridian, its population structure remains poorly understood and needs further investigation. In the Mediterranean Sea, the main spawning areas are located around the Balearic Islands, south Tyrrhenian Sea and Sicily Strait, the Gulf of Sidra and close to Cyprus [ROO 07]. BFT also migrate for feeding purposes within the Mediterranean and the North Atlantic, but movement patterns vary considerably between individuals, years and areas [WAL 09]. BFT display a strong site fidelity for the NW Mediterranean [FRO 14a] and the Ligurian Sea is a well-known nursery and feeding area for juveniles (22°C, [ROO 07]). When the Mediterranean Sea temperature is higher in May–June, both the growth rate and consequently the survival rate of the larvae are higher, as shown by a study comparing the somatic growth of the BFT larvae collected in the Balearics in 2003, an exceptionally warm year, with those collected in 2004 and 2005, years of average temperature [GAR 07]. This higher growth rate and survival effect on the larvae seem to have generated a strong year class in 2003 that has been identified in the fisheriesʼ data a few years later [ICC 13]. Nonetheless, climate-induced changes in lifecycle and behavior remain difficult to document as well as their impacts to predict, since warming affects the whole food chain and thus the complex prey–predator relationships. 5.2.2.2. Small tunas Five of the small tuna species have been recorded in the Ligurian Sea: occasionally, plain bonito (Orcynopsis unicolor) and skipjack tuna (Katsuwonus pelamis), while bullet tuna (Auxis rochei rochei), little tunny (Euthynnus alletteratus) and Atlantic bonito (Sarda sarda), with their regular presence, are commercially exploited [ORS 10a]. Little is known about the biology and ecology of these species that are only exploited by local small-scale fisheries. Even though Atlantic bonito can tolerate cooler water than the other species [BOY 08], most small tunas are warm-water species and should be more abundant with global warming (while other

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predator fish of the NW Mediterranean Sea, such as hake or mackerel, should be adversely affected by warmer waters). Bullet tuna larval stages are ubiquitous and can be found in a wider range of temperatures than other tuna larvae, from 18.5 to 28.5°C, with a preference for temperatures over 23.5°C. As for Bluefin tuna and possibly other small tuna species, temperature has a clear positive influence on the growth rates of this species. Since recruitment variability has been related to early larval and juvenile growth, higher temperatures in the surface layers, inhabited by tuna larva, could result in higher growth rates and higher recruitment, if food is not a limiting factor [PER 09]. 5.2.2.3. Swordfish Recent studies using genetic methods have shown that Mediterranean swordfish compose a unique stock, separate from those of the Atlantic, although information on stock mixing and boundaries remains incomplete [SMI 15]. In the Mediterranean, females mature at around three years (i.e. at about 140 cm), but males reach sexual maturity at smaller sizes and mature specimens have been found at about 90 cm. Knowledge of the reproductive activity of the Mediterranean swordfish is rather limited, but according to past authors, spawning seems to occur in summer and the main spawning grounds occur in the Straits of Sicily and possibly along the Mediterranean Spanish coast and in the Levantine basin [PAL 81, TSE 01]. All life stages were found in the Ligurian Sea, from post-larvae to 11-year-old specimens [GAR 04, ORS 03], thus Garibaldi et al. [GAR 04] hypothesized that swordfish could also spawn in the Pelagos Sanctuary area, which does, however, remain to be confirmed by further studies. Swordfish females, like bluefin tuna, show a strong philopatric behavior towards their respective spawning grounds [ALV 05]. In the Liguria Sea, swordfish feed mainly on mesopelagic fauna; the overall diet composition includes 23 species of fish, 17 cephalopods and six crustaceans, partially overlapping with the diet of the striped dolphin [ORS 95, WÜR 93]. Swordfish make large, vertical excursions to the surface at night and dive as deep as 600 m during the day [CAR 90]. This species has evolved the most functionally distinct and enlarged extraocular muscles in the animal kingdom, that allows them to inhabit and feed in deep cold water on mesopelagic fish and invertebrates. The Ligurian Sea represents one of the

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northernmost areas of its distribution in the Mediterranean, its higher presence there is a possible future scenario. This endothermic ability enables swordfish, like bluefin tuna, to exploit a wide range of oceanic environments. In spite of this capacity, it has been demonstrated that sea surface temperature (SST) is the best single predictor of the abundance of these species, compared with other factors such as oxygen content, prey availability, ocean fronts, zooplankton, salinity, islands, seamounts, etc., suggesting that the water temperature is also an important environmental factor in the case of fishes with thermoregulation capacity [BOY 08]. 5.2.2.4. Mesopelagic fishes According to recent acoustic campaigns, mesopelagic fishes likely dominate the total world fish biomass and their biomass could be 10 times greater than the current estimate thought [IRI 14], most probably that estimation can also be applied to smaller seas such as the Mediterranean Sea or at least to some of its regions (e.g. Ligurian Sea).

Figure 5.3. Mesopelagic fishes. Top: Ruvettus pretiosus, total length (TL) up to 150 cm. Bottom: Centrolophus niger, TL up to 150 cm (drawings by M. Würtz-Artescienza)

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Indeed, we have a very scant picture of the related biomass of the top pelagic predators feeding on mesopelagic prey abundance, and our current knowledge of these fish mostly comes from the bycatches of professional long-line fisheries for swordfish, which provide information on the species, presence in the area. However, such data are so occasional and scattered in time that they are consequently of limited value. In the Ligurian Sea, the main species involved in these kind of fisheries are: oilfish, Ruvettus pretiosus (Figure 5.3 (Top)); rudderfish or blackfish, Centrolophus niger (Figure 5.3 (Bottom)); pomfret, Brama brama (Figure 5.4 (Top)); dolphinfish, Coryphaena hippurus; opah, Lampris guttatus (Figure 5.4 (Bottom)); wreckfish, Polyprion americanus (Figure 5.5 (Top)); sunfish Mola mola; scalloped ribbonfish, Zu cristatus (Figure 5.5 (Bottom)); ribbonfish, Trachipterus trachypterus (Figure 5.6 (Top)); luvar, Luvarus imperialis (Figure 5.6 (Bottom)) and the Paralepidid fish Sudis hyaline (Figure 5.7 (Top)) [GAR 15].

Figure 5.4. Mesopelagic fishes. Top: Brama brama, TL up to 70 cm. Bottom: Lampris guttatus, TL up to 200 cm (drawings by M. Würtz-Artescienza)

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Imperial blackfish (Schedophilus ovalis) (Figure 5.7 (Bottom)) is occasionally recorded. Nevertheless, a large number of young individuals schooling under floating objects are frequently spotted in the Ligurian Sea, during the summer [WÜR 10]. This species is known to have an ontogenetic depth distribution, with young specimens found in the upper layer, from the surface to −50 m, while adults prefer deeper waters, more than 500 m in depth [FRA 03]. The diet of S. ovalis consists of Pyrosoma and other tunicates [HAE 86]. Juveniles of S. ovalis and C. niger are commonly associated with floating jellyfish.

Figure 5.5. Mesopelagic fishes. Top: Polyprion americanus (juv.), TL up to 210 cm. Bottom: Zu cristatus, TL up to 118 cm (drawings by M. Würtz-Artescienza)

Opah (L. guttatus), thanks to its whole-body form of endothermy, is distinctively specialized to exploit cold, deeper waters, maintaining elevated levels of physiological performance. This species has a high thermal tolerance and spends most of its time at depths between 50 and 400 m [WEG 15]. Sunfish (M. mola) appears to be negatively affected by the habit of feeding on jellyfish, the perianal area becoming reddish due to the ingestion of great quantities of Pelagia noctiluca [ORS 10a].

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Many of these species are medusivorous; as jellyfish blooms seem to be driven by climate changes, their increased presence could enhance the abundance of this pelagic species [ARA 05, CAR 12, GAR 04, ORS 10a, ORS 10b]. A possible future scenario foresees a reduction of many species of large pelagic predators, due to the predation of jellyfish on their larval stages and an increase in the medusivorous species [BOE 13]. These species have larval stages that are subjected to jellyfish predation, and the possible effect of this predation is far from being completely investigated.

Figure 5.6. Mesopelagic fishes. Top: Trachipterus trachypterus, TL up to 300 cm. Bottom: Luvarus imperialis, TL up to 200

Other possible effects of climate change could be on both the juvenile stages that live in the superficial layers and whose distribution is most likely linked to the surface temperature, trend of local currents, and on adults, in the case of important temperature variations of the intermediate layers of the water column, for example recent Levantine intermediate water (LIW) warming.

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Figure 5.7. Mesopelagic fishes. Top: Sudis hyaline, TL up to 100 cm. Bottom: Schedophilus ovalis, TL up to 100 cm (drawings by M. Würtz-Artescienza)

5.2.3. Sharks and rays A number of pelagic shark species inhabit the Mediterranean Sea and visit the NW Mediterranean (including the Ligurian Sea) for short to long periods, mostly for feeding purposes. The main species are Prionace glauca (blue shark), Isurus oxyrinchus (shortfin mako), Alopias vulpinus (common thresher), A. superciliosus (bigeye thresher), Lamna nasus (porbeagle), Carcharodon carcharias (great white shark), Cetorhinus maximus (basking shark) and some species of Sphyrna and Carcharhinus genera [COM 84]; the giant devil ray (Mobula mobular) and pelagic stingray (Pteroplatytrygon violacea), though not so frequently, are commonly sighted during summer. Declines in several pelagic sharks in the north-western Mediterranean have been as due to fishing documented by Ferretti et al. [FER 08]. In the Ligurian Sea, the presence of some shark species (P. glauca, A. vulpinus, L. nasus, I. oxyrinchus and Sphyrna spp.) as been dramatically reduced in the catches of different fishing gears since the early 20th Century, so that these populations are considered to have been significantly depleted. In 2010, the new mesopelagic long line was introduced in the Ligurian Sea swordfish fishery, resulting in more effective catches of swordfish with great

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reductions in bycatches; among the elasmobranchs, only blue shark and little sleeper shark (Somniosus rostratus) have been recorded [GAR 15]. Basking sharks (C. maximus) locate and remain within productivity “hot-spots” occurring seasonally along large-scale frontal features. They forage selectively on specific zooplankton assemblages [SIM 03] and seem to be philopatric, showing a tendency to return every year to the same feeding locations. In the Mediterranean, basking shark distribution could be related to surface water temperature, wind speed, surface currents and average chlorophyll concentration. A potential aggregation site corresponds to the Cetacean Sanctuary in the Ligurian Sea. The return of basking sharks to these waters in the spring is probably associated with periods of high biological production and particularly northern krill (Meganyctiphanes norvegica) swarms. Currently, no clear evidence of climate-change effects on Mediterranean shark populations has been found, particularly on pelagic sharks. Nevertheless, it is possible that the sharp decline of fishing due to the pressure of fishing and habitat degradation, have masked variation trends in their distribution, predatory behavior, rate of reproduction and shift of spawning grounds. On the contrary, Rosa et al. [ROS 17], who studied the effect of global ocean acidification (OA) on pelagic sharks, found that elevated CO2 has clear effects on body condition, growth, aerobic potential and behavior (e.g. lateralization, hunting and prey detection), suggesting that the effects of OA could be greater than those due to warming. The modification of predator behavior can have large effects on trophically structured systems like the Ligurian Sea. Although embryonic development is accelerated as temperature increases, elevated temperature and CO2 had detrimental effects on sharks by increasing energetic demands, by decreasing metabolic efficiency and reducing their ability to locate food through olfaction. In elevated CO2 environments, sharks could show a considerable reduction in growth rate, and their ability to hunt, thus lessening strong top-down control over food webs [PIS 15]. 5.2.4. Sea turtles The Mediterranean region is an important breeding area for the loggerhead turtle (Caretta caretta) and green turtle (Chelonia mydas).

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The leatherback turtle (Dermochelys coriacea) is distributed across the whole region, although no regular reproduction has been observed [CAS 03]. Hawksbill turtle (Eretmochelys imbricata) and Kemp’s ridley turtle (Lepidochelys kempii) have also been occasionally recorded [INS 10, LAU 91, TOM 08]. Loggerhead is the most abundant sea turtle in Mediterranean waters and its distribution extends from the eastern to the western basins, including the Black Sea [CAS 18]. On the contrary, green turtles seem to be mostly restricted to the eastern basin, as few specimens have been recorded in the western Mediterranean, and in particular in the Ligurian Sea [BEN 11, LES 15]. Up to now, most of the nesting sites have been identified on beaches of the eastern and south-central Mediterranean. Sporadic cases have been reported in Croatia, on the Italian Adriatic coast and in southern Spain. The northernmost nesting sites of loggerheads have been discovered near St. Tropez in 2006 [SEN 09] and on the beach of Villeneuve-les-Maguelones, France in 2018, as well as new born loggerheads documented on the beaches of Elba Island, and in June 2019, a nest documented on the beach of Cecina (Italy, Tyrrhenian Sea). The migratory behavior of loggerhead turtles in the Mediterranean Sea is characterized by considerable complexity. The Adriatic and Libyan– Tunisian shelves represent key neritic foraging areas both for adults and juveniles. Nevertheless, offshore waters may be an important foraging area for specimens in their inter-reproductive phase. Juveniles have also been found to perform diverse movement patterns, being erratic over pelagic or neritic areas, prolonging their stays in restricted zones or even migrating seasonally over long distances [LUS 14]. Mediterranean loggerhead turtles have also been seen to remain in the northernmost and coldest part of the basin during the whole winter [CAS 18], by adopting the so-called overwintering strategy [HOC 07], thus cold winter temperatures drive only some adult and juvenile loggerheads to move southward from the Ligurian Sea and the northern Adriatic Sea [LUS 14]. Loggerhead sea turtle specimens from the Atlantic Ocean are known to migrate into the Mediterranean Sea; they mostly congregate in oceanic waters of the southern part of the western basin, Sicily Channel and North Ionian Sea, as well as in the neritic zone of the Tunisian shelf. As the genetic

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flow from the Atlantic to the Mediterranean has been estimated to be low, it is likely these Atlantic turtles do not breed in the Mediterranean, but return to the Atlantic for reproduction [CAM 04, CAR 11]. As ectothermic species, the sea turtles can be affected by environmental temperatures, thus climate change can influence their foraging behavior, migratory patterns, sex ratio and breeding success. Sea turtles have temperature-dependent sex determination, warmer temperatures produce more females and cooler temperatures give more males. Nowadays, nests seem to be normally female-biased, an increasing sand temperature associated with climate change may lead to an even higher proportion of female hatchlings and a shortage of males. Unsuitable temperatures may also have a negative impact on the hatching success, which may be low below approximately 25°C and above 35°C [HAW 14]. Climate change may reduce the availability of suitable nesting beaches, not only because of the temperature variation, but also by other effects such as the sea level rising and coastal erosion, in combination with lots of natural beaches, because of human developments. In the simplest case scenario, a sea level rise and coastal erosion would mean that a typical nesting beach would be inundated higher up the shoreline, reducing the net area available for egg laying and successful incubation [HAW 14]. On the contrary, marine turtles seem to adapt their nesting behavior to the changing climate by laying eggs earlier in the season or at higher latitudes [MAZ 13]. Evidence exists that marine turtles are able to colonize both newly formed natural and artificial beaches. As loggerhead turtles are now nesting at their furthest north since records began, it seems that the sites that were previously too cool for successful incubation may be opened to nesting by climate change [BEN 10, MAF 16, SEN 09]. 5.2.5. Marine mammals The Ligurian Sea is a hotspot for marine mammals in the Mediterranean Sea, which led, in 2005, to the establishment of a high seas marine protected area, the Pelagos Sanctuary for Mediterranean marine mammals, which covers about 87,500 km2 between the Italian and French coasts and the northern coast of Sardinia. In this area, several species of cetaceans find favorable conditions for feeding and reproduction; among these, the most

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frequent species, with typically pelagic habits, are the fin whale (Balaenoptera physalus), the sperm whale (Physeter catodon), the striped dolphin (Stenella coeruleoalba), the Risso’s dolphin (Grampus griseus), the long-finned pilot whale (Globicephala melas) and the Cuvier’s beaked whale (Ziphius cavirostris). The bottlenose dolphin (Tursiops truncatus) is also a common species but mostly confined within neritic waters, while the short beaked common dolphin (Delphinus delphis) is sighted with less frequency, often associated with striped dolphin herds. Some of these species are (almost) resident in the Pelagos sanctuary, while others (e.g. sperm whale and fin whale) only migrate seasonally in this area. The monk seal (Monachus monachus), once present in the Ligurian Sea, as evidenced by a specimen displayed at the Museum of Natural History of Genoa – an adult female caught in the tuna trap of Camogli in 1935 – is now an extremely rare and exceptional presence. The impacts of climate change on cetaceans can be diverse and mediated in various ways, some may be direct: for example, as temperatures change, some cetacean species may respond by shifting their distributions to remain within optimal habitat. However, in some cases, such as in the Mediterranean, the range shifts will not be possible or will be very limited, so difficult to detect. Climate change will also have indirect impacts, a probable increase in susceptibility to disease and contaminants [PHI 11] and changes in the availability and abundance of food resources, particularly for fin whales, which primarily feed on the northern krill (Meganyctiphanes norvegica, see Chapter 4). Cetaceans are already facing numerous non-climate related threats, such as chemical and noise pollution, commercial fishing, commercial shipping, naval activities, etc. which can reduce their adaptive capacity [ELL 07]. Relatively few studies document the effect of climate variation on cetacean species considering local scales [AZZ 08]; however, as the cetaceans are eurythermic, it can be supposed that their response might be an indirect effect of climate change on the availability of their prey. Sea surface temperature (SST) and thermal fronts have been described as factors of influence for cetacean distribution [HAS 05, TYN 05]. According to Azzellino et al. [AZZ 08], striped dolphins and fin whales avoid SST extreme values, instead preferred by sperm whales. These results allow the conclusion that cetacean distribution in the western Ligurian Sea may change in response to climate variability; however, other factors such as

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seamounts and submarine canyons seem to have a stronger effect in aggregating some cetacean species, for example striped dolphin and sperm whale [FIO 16]. As cetaceans exploit a large variety of mesopelagic prey, shifts of the physical and biological characteristics in the intermediate water environment may have effects. During the summer of 2016, a sharp reduction in sightings of many species of cetaceans was observed, when the temperature of the LIW was particularly high (Bozzo – Whale Watching company and Aps Menkab, personal communications). Such a unique observation is obviously too limited to draw any conclusion, but it would be of interest to investigate potential mechanisms between the physical properties of the LIW, the abundance of the mesopelagic fauna and the local abundance of marine mammals in the Ligurian Sea. In fact, the underlying mechanisms of the effects on higher trophic levels remain unclear [STE 03], in particular when considering cetaceans, which, as mammals, certainly behave more complexly than other predators living in the same environment. Furthermore, relationships may not be linear, and therefore, even more difficult to understand. There may be lags in the responses to local climate variations [HAL 04] which coupled with other nonlinear dynamics (i.e. cultural transmission within and through herds), make it even more difficult to understand the patterns. 5.3. Conclusion Closely adjacent submarine canyons, seamounts and steep slopes affect the cyclonic circulation by altering the direction of the flow in a variable way according to its seasonal intensity making the pelagic realm of the Ligurian Sea a highly variable and heterogeneous environment [WÜR 12, WÜR 15]. Consequently, it is difficult to identify the main factors (which further interact) that drive variation in abundances of the population of a given resident or transient top predator species. The Ligurian Sea is one of the most studied areas of the Mediterranean Sea, and we possess a contemporary picture of its circulation as well as of biological processes, species presence and distribution. Nevertheless, the mechanisms regulating the life in the water column between the surface and the deepest seafloor, its largest habitat, are still little known. The Ligurian

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Sea offers suitable conditions for feeding and reproduction of many top pelagic predators. Such predators have a huge appetite that is satisfied by a great and variable number of prey, mainly pelagic and mesopelagic crustaceans, cephalopods and fishes, but some are adapted to feed on jellyfishes. Currently, it is believed that the top predators in the Ligurian Sea are sustained by some key species: northern krill, the euphausid, M. norvegica; cephalopods, mainly two species, Histioteuthis bonnellii and H. reversa; small pelagic fishes (mainly anchovy, sardine and blue whiting) and small mesopelagic fishes (mainly myctophids). Certainly, the trophic pathways of some predators are much more complex, otherwise we can explain their presence in a sea with such distinct oligotrophic characteristics. The seasonal peaks of chlorophyll at the core of the Ligurian Sea are not enough to explain this abundance; other mechanisms could act in the production processes, likely involving microbes and jellyfishes [DAL 16, JAC 89, KAR 99, POM 01]. The complexity of processes, which give the Mediterranean Sea its peculiar carrying capacity and high biodiversity level, is based on a close relationship between factors not yet fully explained; moreover, this dynamic balance appears more and more fragile, in light of the increasing human pressure along its shores and within its basin. The future scenario of the combined contribution of climate change and other anthropic impacts on a local scale in the Mediterranean Sea will most probably act faster than in other regions of the global ocean. Unfortunately, as far as the top pelagic predators are concerned, we must conclude that underlying causes of increase or depletion are difficult to examine rigorously due to highly variable, spatially and temporally limited data [BAU 09]. 5.4. Acknowledgments We are grateful to Sandra Hochscheid, head of Aquarium Unit and of Marine Turtle Research Center, Stazione Zoologica Anton Dohrn, for revising the text on sea turtles and for valuable bibliographical suggestions. We also thank our colleagues Christophe Migon, Jean-Olivier Irisson and Antoine Sciandra. Laboratoire d’Océanographie de Villefranche, for having followed the work of revision and layout. Finally, a heartfelt acknowledgment of the anonymous reviewers of the English version of the text.

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5.5. References [ALB 12] ALBOUY C., GUILHAUMON F., ARAUJO M.B. et al., “Combining projected changes in species richness and composition reveals climate change impacts on coastal Mediterranean fish assemblages”, Global Change Biology, vol. 18, pp. 2995–3003, 2012. [ALV 05] ALVARO BREMER J.R., VINAS J., MEJUTO J. et al., “Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes”, Molecular Phylogenetics and Evolution, vol. 36, pp. 169–187, 2005. [ARA 05] ARAI M.N., “Predation on pelagic coelenterates: A review”, Journal of the Marine Biological Association of the United Kingdom, vol. 85, pp. 523–536, 2005. [AZZ 08] AZZELLINO A., GASPARI S.A., AIROLDI S. et al., “Biological consequences of global warming: Does sea surface temperature affect cetacean distribution in the western Ligurian Sea?”, Journal of the Marine Biological Association of the United Kingdom, vol. 88, pp. 1145–1152, 2008. [AZZ 11] AZZURRO E., MOSCHELLA P., MAYNOU F., “Tracking signals of change in Mediterranean fish diversity based on local ecological knowledge”, Plos One, vol. 6, pp. 1–8, 2011. [BAU 09] BAUM J.K., WORM B., “Cascading top-down effects of changing oceanic predator abundances”, Journal of Animal Ecology, vol. 78, pp. 699–714, 2009. [BEL 99] BELLO G., BIAGI V., “A large cranchiid squid (Cephalopoda: Teuthoidea) caught in the Mediterranean Sea”, Bollettino Malacologico, vol. 34, pp. 69–70, 1999. [BEN 09] BEN RAIS LASRAM F., MOUILLOT D., “Increasing southern invasion enhances congruence between endemic and exotic Mediterranean fish fauna”, Biological Invasions, vol. 11, pp. 697–711, 2009. [BEN 10] BENTIVEGNA F., RASOTTO M.B., DE LUCIA G.A. et al., “Loggerhead turtle (Caretta caretta) nests at high latitudes in Italy: A call for vigilance in the Western Mediterranean”, Chelonian Conservation and Biology, vol. 9, pp. 283–289, 2010. [BEN 11] BENTIVEGNA F., CIAMPA M., HOCHSCHEID S., “The presence of the green turtle, Chelonia mydas, in Italian coastal waters during the last two decades”, Marine Turtle Newsletter, pp. 41–46, 2011.

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[BLO 05] BLOCK B.A., TEO S.L.H., WALLI A. et al., “Electronic tagging and population structure of Atlantic bluefin tuna”, Nature, vol. 434, pp. 1121–1127, 2005. [BOE 13] BOERO F., “Review of jellyfish blooms in the Mediterranean and Black Sea”, in Studies and Reviews. General Fisheries Commission for the Mediterranean, FAO, Rome, 2013. [BOY 08] BOYCE D.G., TITTENSOR D.P., WORM B., “Effects of temperature on global patterns of tuna and billfish richness”, Marine Ecology Progress Series, vol. 355, pp. 267–276, 2008. [CAL 11] CALVO E., SIMO R., COMA R. et al., “Effects of climate change on Mediterranean marine ecosystems: The case of the Catalan Sea”, Climate Research, vol. 50, pp. 1–29, 2011. [CAM 04] CAMIÑAS J.A., DE MÁLAGA C.O., “Sea turtles of the Mediterranean Sea: Population dynamics, sources of mortality and relative importance of fisheries impacts”, FAO Fisheries Report, vol. 738 Suppl, pp. 27–84, 2004. [CAR 90] CAREY F.G., “Further acoustic telemetry observations of swordfish – Planning the future of billfishes”, Proceedings of the second International Billfish Symposium, Part 2, National Coalition for Marine Conservation, 1990. [CAR 11] CARRERAS C., PASCUAL M., CARDONA L. et al., “Living together but remaining apart: Atlantic and Mediterranean loggerhead sea turtles (Caretta caretta) in shared feeding grounds”, Journal of Heredity, vol. 102, pp. 666–677, 2011. [CAR 12] CARDONA L., DE QUEVEDO I.A., BORRELL A. et al., “Massive consumption of gelatinous plankton by Mediterranean apex predators”, Plos One, vol. 7, no. 3. doi: 10.1371/journal.pone.0031329, 2012. [CAS 03] CASALE P., NICOLOSI P., FREGGI D. et al., “Leatherback turtles (Dermochelys coriacea) in Italy and in the Mediterranean basin”, Herpetological Journal, vol. 13, pp. 135–139, 2003. [CAS 18] CASALE P., BRODERICK A.C., CAMINAS J.A. et al., “Mediterranean sea turtles: Current knowledge and priorities for conservation and research”, Endangered Species Research, vol. 36, pp. 229–267, 2018. [COL 01] COLLETTE B.B., REEB C., BLOCK B.A., “Systematics of the tunas and mackerels (Scombridae)”, in BLOCK B.A., STEVENS E.D. (eds), Fish Physiology, Academic Press, San Diego, 2001. [COL 10] COLL M., PIRODDI C., STEENBEEK J. et al., “The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats”, Plos One, vol. 5, no. 8. doi: 10.1371/journal.pone.0011842, 2010.

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[COM 84] COMPAGNO L.J.V., “An annotated and illustrated catalogue of shark species known to date”, FAO Fish. Synop. 125, vol. 4, p. 655, 1984. [COM 09] COMA R., RIBES M., SERRANO E. et al., “Global warming-enhanced stratification and mass mortality events in the Mediterranean”, Proceedings of the National Academy of Sciences of the United States of America, vol. 106, pp. 6176–6181, 2009. [DAL 16] D'ALELIO D., LIBRALATO S., WYATT T. et al., “Ecological-network models link diversity, structure and function in the plankton food-web”, Scientific Reports, vol. 6, pp. 1–13, 2016. [DAN 09] DANOVARO R., UMANI S.F., PUSCEDDU A., “Climate change and the potential spreading of marine mucilage and microbial pathogens in the Mediterranean Sea”, Plos One, vol. 4, no. 9, 2009. doi: 10.1371/ journal.pone.0007006. [DRU 11] DRUON J.N., FROMENTIN J.M., AULANIER F. et al., “Potential feeding and spawning habitats of Atlantic bluefin tuna in the Mediterranean Sea”, Marine Ecology Progress Series, vol. 439, pp. 223–240, 2011. [ELL 07] ELLIOTT W., SIMMONDS M.P., Whales in Hot Water: The Impact of a Changing Climate on Whales, Dolphins and Porpoises: A Call for Action, World Wildlife Fund International, Gland Switzerland/WDCS, Chippenham, UK, 2007. [EVA 15] EVANS J., BARBARA J., SCHEMBRI P.J., “Updated review of marine alien species and other ‘newcomers’ recorded from the Maltese Islands (Central Mediterranean)”, Mediterranean Marine Science, vol. 16, pp. 225–244, 2015. [FER 08] FERRETTI F., MYERS R.A., SERENA F. et al., “Loss of large predatory sharks from the Mediterranean Sea”, Conservation Biology, vol. 22, pp. 952–964, 2008. [FIO 16] FIORI C., PAOLI C., ALESSI J. et al., “Seamount attractiveness to top predators in the southern Tyrrhenian Sea (central Mediterranean)”, Journal of the Marine Biological Association of the United Kingdom, vol. 96, pp. 769–775, 2016. [FRA 03] FRANCOUR P., JAVEL F., “Recent occurrences of young Schedophilus ovalis (Centrolophidae) along French Mediterranean coasts”, Cybium, vol. 27, pp. 57–58, 2003. [FRO 05] FROMENTIN J.M., POWERS J.E., “Atlantic bluefin tuna: Population dynamics, ecology, fisheries and management”, Fish and Fisheries, vol. 6, pp. 281–306, 2005. [FRO 09] FROMENTIN J.M., “Lessons from the past: Investigating historical data from bluefin tuna fisheries”, Fish and Fisheries, vol. 10, pp. 197–216, 2009.

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[INS 10] INSACCO G., SPADOLA F., “First record of Kemp's ridley sea turtle, Lepidochelys kempii (Garman, 1880) (Cheloniidae), from the Italian waters (Mediterranean Sea)”, Acta Herpetologica, vol. 5, pp. 113–117, 2010. [IRI 14] IRIGOIEN X., KLEVJER T.A., ROSTAD A. et al., “Large mesopelagic fishes biomass and trophic efficiency in the open ocean”, Nature Communications, vol. 5, pp. 1–10, 2014. [JAC 89] JACQUES G., “L'oligotrophie du milieu pélagique de Méditerranée occidentale: un paradigme qui s' éstompe?”, Bulletin de la Société zoologique de France, vol. 114, pp. 17–30, 1989. [KAR 99] KARL D.M., “A sea of change: Biogeochemical variability in the North Pacific Subtropical Gyre”, Ecosystems, vol. 2, pp. 181–214, 1999. [KEL 17] KELLER S., QUETGLAS A., PUERTA P. et al., “Environmentally driven synchronies of Mediterranean cephalopod populations”, Progress In Oceanography, vol. 152, pp. 1–14, 2017. [KNI 15] KNITTWEIS L., “Economic and labour market implications of climate change on the fisheries sector of the Maltese Islands”, Xjenza Online, vol. 3, pp. 118–127, 2015. [LAU 91] LAURENTAND L., LESCURE J., “Hawksbill turtles in the Mediterranean Sea”, Marine Turtle Newsletter, vol. 54, pp. 12–13, 1991. [LEJ 10] LEJEUSNE C., CHEVALDONNE P., PERGENT-MARTINI C. et al., “Climate change effects on a miniature ocean: The highly diverse, highly impacted Mediterranean Sea”, Trends in Ecology & Evolution, vol. 25, pp. 250–260, 2010. [LES 15] LESCURE J., CATEAU S., SENEGAS J.-B. et al., “Présence de la Tortue verte, Chelonia mydas (Linnaeus, 1758), en Méditerranée française”, Bulletin de la Société Herpétologique de France, vol. 156, pp. 1–14, 2015. [LUS 14] LUSCHI P., CASALE P., “Movement patterns of marine turtles in the Mediterranean Sea: A review”, Italian Journal of Zoology, vol. 81, pp. 478–495, 2014. [MAC 13] MACIAS D., GARCIA-GORRIZ E., STIPS A., “Understanding the causes of recent warming of Mediterranean waters. How much could be attributed to climate change?”, Plos One, vol. 8, pp. 1–6, 2013. [MAC 14] MACKENZIE B.R., PAYNE M.R., BOJE J. et al., “A cascade of warming impacts brings bluefin tuna to Greenland waters”, Global Change Biology, vol. 20, pp. 2484–2491, 2014. [MAF 16] MAFFUCCI F., CORRADO R., PALATELLA L. et al., “Seasonal heterogeneity of ocean warming: A mortality sink for ectotherm colonizers”, Scientific reports, vol. 6, pp. 1–9, 2016.

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[MAU 05] MAURY O., LEHODEY P., Climate Impacts on Oceanic Top Predators (CLIOTOP): Science Plan and Implementation Strategy, Climate Impacts on Oceanic TOp Predators (CLIOTOP). Science Plan and Implementation Strategy, GLOBEC 2005. [MAZ 13] MAZARIS A.D., KALLIMANIS A.S., PANTIS J.D. et al., “Phenological response of sea turtles to environmental variation across a speciesʼ northern range”, Proceedings of the Royal Society B – Biological Sciences, vol. 280, pp. 1–9, 2013. [MUH 11] MUHLING B.A., LEE S.K., LAMKIN J.T. et al., “Predicting the effects of climate change on bluefin tuna (Thunnus thynnus) spawning habitat in the Gulf of Mexico”, Ices Journal of Marine Science, vol. 68, pp. 1051–1062, 2011. [ORS 94] ORSI-RELINI L., RELINI G., CIMA C. et al., “Meganyctiphanes norvegica and fin whales in the Ligurian Sea: New seasonal patterns”, European Research on Cetaceans, vol. 8, pp. 179–182, 1994. [ORS 95] ORSI-RELINI L., GARIBALDI F., CIMA C. et al., “Feeding of the swordfish, the bluefin and other pelagic nekton in the Western Ligurian Sea”, Collective Volume of Scientific Pappers ICCAT, vol. 44, pp. 283–286, 1995. [ORS 03] ORSI-RELINI L., PALANDRI G., GARIBALDI F., “Reproductive parameters of the Mediterranean swordfish”, Biologia Marina Mediterranea, vol. 10, pp. 210–222, 2003. [ORS 10a] ORSI-RELINI L., GARIBALDI F., LANTERI L. et al., “Medusivorous fishes of the Ligurian Sea 1. Chub mackerels and other pelagic fish species sometimes “have the medusa” Pelagia noctiluca”, Rapports CIESM, vol. 39, p. 612, 2010. [ORS 10b] ORSI-RELINI L., PALANDRI G., RELINI M., “Medusivorous fishes of the Ligurian Sea 3. The young giant, Mola mola at the Camogli tuna trap”, Rapports CIESM, vol. 39, p. 613, 2010. [PAC 15] PACE D.S., TIZZI R., MUSSI B., “Cetaceans value and conservation in the Mediterranean Sea”, Journal of Biodiversity & Endangered Species, vol. 3, pp. 1–24, 2015. [PAL 81] PALKO B.J., BEARDSLEY G.L., RICHARDS W.J., “Synopsis of the biology of the swordfish, Xiphias gladius Linnaeus (L)”, U.S. Dep. Commer., NOAA Tech. Rep. NMFS Circ., 1981. [PEC 06] PECL G., JACKSON G., “How climate change may influence loliginid squid populations”, in The Role of Squid in Pelagic Marine Ecosystems, GLOBEC-CLIOTOP WG3 Workshop, University of Hawaii, Manoa, 2006.

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[PER 09] PÉREZ-TORRES A., ALEMANY F., REGLERO P., “Environmental variability on the distribution, abundances and growth rates of the larvae of bullet tuna”, ICES CM, 2009. [PHI 11] PHILIPPART C.J.M., ANADON R., DANOVARO R. et al., “Impacts of climate change on European marine ecosystems: Observations, expectations and indicators”, Journal of Experimental Marine Biology and Ecology, vol. 400, pp. 52–69, 2011. [PIE 08] PIERCE G.J., VALAVANIS V.D., GUERRA A. et al., “A review of cephalopodenvironment interactions in European Seas”, Hydrobiologia, vol. 612, pp. 49–70, 2008. [PIE 10] PIERCE G.J., ALLCOCK L., BRUNO I. et al., “Cephalopod biology and fisheries in Europe”, ICES Cooperative Research Report, vol. 303, pp. 175, Copenhagen, Denmark, 2010. [PIS 15] PISTEVOS J.C.A., NAGELKERKEN I., ROSSI T. et al., “Ocean acidification and global warming impair shark hunting behaviour and growth”, Scientific reports, vol. 5, pp. 1–10, 2015. [POM 01] POMEROY L.R., “Caught in the food web: Complexity made simple?”, Scientia Marina, vol. 65, pp. 31–40, 2001. [PSO 11] PSOMADAKIS P.N., BENTIVEGNA F., GIUSTINO S. et al., “Northward spread of tropical affinity fishes: Caranx crysos (Teleostea: Carangidae), a case study from the Mediterranean Sea”, Italian Journal of Zoology, vol. 78, pp. 113–123, 2011. [QUE 04] QUETGLAS A., MORALES-NIN B., “Age and growth of the ommastrephid squid Todarodes sagittatus from the Western Mediterranean Sea”, Journal of the Marine Biological Association of the United Kingdom, vol. 84, pp. 421–426, 2004. [RAG 02] RAGONESE S., JEREB P., DAWE E., “A comparison of growth performance across the squid genus Illex (Cephalopoda, Ommastrephidae) based on modelling weight-at-length and age data”, Journal of Shellfish Research, vol. 21, pp. 851–860, 2002. [RAI 10] RAITSOS D.E., BEAUGRAND G., GEORGOPOULOS D. et al., “Global climate change amplifies the entry of tropical species into the Eastern Mediterranean Sea”, Limnology and Oceanography, vol. 55, pp. 1478–1484, 2010. [RAV 04] RAVIER C., FROMENTIN J.M., “Are the long-term fluctuations in Atlantic bluefin tuna (Thunnus thynnus) population related to environmental changes?”, Fisheries Oceanography, vol. 13, pp. 145–160, 2004.

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[RIX 05] RIXEN M., BECKERS J.M., LEVITUS S. et al., “The Western Mediterranean deep water: A proxy for climate change”, Geophysical Research Letters, vol. 32, pp. 1–4, 2005. [ROO 07] ROOKER J.R., BREMER J.R.A., BLOCK B.A. et al., “Life history and stock structure of Atlantic bluefin tuna (Thunnus thynnus)”, Reviews in Fisheries Science, vol. 15, pp. 265–310, 2007. [ROS 17] ROSA R., RUMMER J.L., MUNDAY P.L., “Biological responses of sharks to ocean acidification”, Biology Letters, vol. 13, pp. 1–7, 2017. [SCH 16] SCHROEDER K., CHIGGIATO J., BRYDEN H.L. et al., “Abrupt climate shift in the Western Mediterranean Sea”, Scientific Reports, vol. 6, pp. 1–4, 2016. [SEN 09] SÉNÉGAS J.-B., HOCHSCHEID S., GROUL J.-M. et al., “Discovery of the northernmost loggerhead sea turtle (Caretta caretta) nest”, Marine Biodiversity Records, vol. 2, pp. 1–4, 2009. [SHA 14] SHALTOUT M., OMSTEDT A., “Recent sea surface temperature trends and future scenarios for the Mediterranean Sea”, Oceanologia, vol. 56, pp. 411–443, 2014. [SIM 03] SIMS D.W., SOUTHALL E.J., RICHARDSON A.J. et al., “Seasonal movements and behaviour of basking sharks from archival tagging: No evidence of winter hibernation”, Marine Ecology Progress Series, vol. 248, pp. 187–196, 2003. [SMI 15] SMITH B.L., LU C.P., GARCIA-CORTES B. et al., “Multilocus Bayesian estimates of intra-oceanic genetic differentiation, connectivity, and admixture in Atlantic swordfish (Xiphias gladius L.)”, Plos One, vol. 10. doi: 10.1371/journal.pone.0127979, 2015. [STE 03] STENSETH N.C., OTTERSEN G., HURRELL J.W. et al., “Studying climate effects on ecology through the use of climate indices: The North Atlantic Oscillation, El Nino Southern Oscillation and beyond”, Proceedings of the Royal Society B – Biological Sciences, vol. 270, pp. 2087–2096, 2003. [TOM 08] TOMÁS J., RAGA J.A., “Occurrence of Kemp's ridley sea turtle (Lepidochelys kempii) in the Mediterranean”, Marine Biodiversity Records, vol. 1, pp. 1–2, 2008. [TSE 01] TSERPES G., PERISTERAKI P., SOMARAKIS S., “On the reproduction of swordfish (Xiphias gladius L.) in the Eastern Mediterranean”, Collective Volume of Scientific Papers ICCAT, vol. 52, pp. 740–744, 2001. [TYN 05] TYNAN C.T., AINLEY D.G., BARTH J.A. et al., “Cetacean distributions relative to ocean processes in the northern California Current System”, Deep-Sea Research Part II – Topical Studies in Oceanography, vol. 52, pp. 145–167, 2005.

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6 A Biogeochemical Approach to Contamination of the Ligurian Sea

6.1. Introduction In this chapter, we review the occurrence, concentrations, biogeochemical behaviors and fluxes of the main categories of chemical contaminants in the Ligurian Sea (LS), namely trace metals – with a special focus on mercury (Hg) and tributyltin (TBT) – anthropogenic radionuclides and organic chemical contaminants (OCCs). We focus on offshore areas, since the nearshore contamination is heterogeneous and spotty (with high concentration gradients) and should be assessed locally. However, continental sources will be discussed on an ad hoc basis. We avoid a tedious catalog of concentrations in the various compartments of the LS ecosystem, and focus our review on the biogeochemical aspects that control the bioavailability of chemical contaminants. While the Tuscan Archipelago constitutes a frontal zone, the LS and Gulf of Lion are particularly well interconnected via the Northern Current and are considered as a single epipelagic biogeochemical region. The vertical structure of the LS can be subdivided into three parts: (1) surface waters (0–200 m) constituted by the modified Atlantic water (MAW), (2) intermediate waters (200–800 m) constituted by the Levantine intermediate water (LIW), the Tyrrhenian dense water (TDW) and the autochthonous winter intermediate water (WIW), and (3) the western Chapter written by Daniel COSSA, Scott W. Lars-Éric HEIMBÜRGER-BOAVIDA and Aurélie DUFOUR.

FOWLER,

The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

Christophe

MIGON,

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Mediterranean deep water (WMDW), which extends to the bottom (approximately 2800 m). The major feature of the hydrological circulation is a coastal cyclonic gyre, which concerns the entire water column (see Volume 1, Chapter 3 of this book series). In addition, the LS is a semi-enclosed basin with a narrow continental shelf (see Volume 1, Chapter 2 of this book series); thus, the nearshore areas receive direct continental runoffs with their convoy of chemical contaminants. From a chemical contamination point of view, the coastal LS is characterized by a highly urbanized and industrialized coastline with high ship traffic, including large harbors and major cities such as Nice, Savona, Genoa, La Spezia and Livorno. However, the western part of the LS is a real oceanic system, where the major chemical inputs are atmospherically transported from land-based sources. The Northern Current isolates the most distant part of the LS from direct contamination from the rare riverine inputs. The eastern part of the LS includes a continental platform that may reach 70 km in width. The regions studied in this chapter are shown in Figure 6.1 with sampling stations.

Figure 6.1. Sampling stations: Antares (42°48’10’’N, 06°07’29”E; bottom: 2497 m), Dy (43°25’N, 07°52’E; bottom: 2350 m), BOA (43°48.9’N, 09°06.8’E; bottom: 1900 m), Tyr-1 (39°52’07”N, 12°49’25”E; bottom: 3180 m) and Tyr-9 (39°55’N, 14°00’E; bottom: 2364 m)

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6.2. Trace metal contamination 6.2.1. Impact of atmospheric deposition Many studies have reported that atmospheric deposition is the most efficient transport route to spread a wide variety of compounds, including contaminants, over open waters (e.g. [WEI 17]). This is particularly true in the case of the Mediterranean (Med), the shores of which are densely populated (approximately 300 inhabitants per km2), with intense and varied land-based emission sources. This results in significant particulate and dissolved fluxes of contaminants deposited at the sea surface, including trace metals (TMs). In the W Med, the most significant inputs of contaminants generally occur in March, due to the advective transport of polluted air masses from Europe, and even more during September–October, presumably due to the autumnal equinox that indicates the shifting of the polar front southwards, which yields the arrival of air masses originating from the N– NE industrialized regions of Europe [BAR 04]. The LS is affected by anthropogenic (mostly from NE and central Europe) and natural (from Saharan regions) atmospheric inputs. Thus, TM concentrations in Ligurian surface waters are higher than those, for example, in the Atlantic Ocean. However, the actual impact of atmospheric loads on marine TM concentrations in the LS remains poorly documented. The first problem to be addressed is whether the residence time (RS) of the surface waters of the LS is long enough to allow atmospheric inputs to significantly change surface TM concentrations. The surface flux (0–200 m) of Atlantic waters ascending along the NW coast of Corsica is 17.3 × 1012 m3 per year. The mixing of this flux with waters originating from the Tyrrhenian Sea (20.5 × 1012 m3 yr−1) generates the Northern Current that exits the LS with a water flow of 37.8 × 1012 m3 yr−1. Thus, considering the surface area of the LS (here 0.53 × 1011 m2), we can deduce that, for a 200 m-thick surface layer, the volume V of surface waters is equal to 0.53 × 1011 × 200 = 10.6 × 1012 m3. Apart from short episodes of dense water formation in winter, the RT of the surface layer of the LS can be computed as: RS = V/(37.8 × 1012) = 0.28 years = 102 days This period of time is long enough to allow the formation of a homogeneous water body. It is therefore justified to address the impact of atmospheric fluxes of contaminants on dissolved marine concentrations. It is

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increasingly accepted that, apart from the “flushdown effect” caused by winter convection [HEI 14], atmospheric matter is efficiently transferred to the seabed, but only under the conditions of biological productivity by its packaging with large biogenic particles [FOW 87, MIG 02]. For this reason, Heimbürger et al. [HEI 11] limited their impact study to the period of water column stratification (spring–autumn), when the downward transfer is minimum and atmospheric matter accumulates in the surface layer. As the stratification develops, the mixed layer becomes thinner and decreases from approximately 30 m thickness (March) to approximately 10 m thickness (May), with low interannual variability. Heimbürger et al. [HEI 11] computed the impact of atmospheric deposition within a 10–30 m-thick surface layer corresponding to a homogeneous mixed layer using literature data (seawater-labile atmospheric inputs of TMs and TM dissolved concentrations in the 0–200 m surface layer). The results (mean situations) are summarized in Table 6.1. Higher enrichment may be expected over shorter spatial and temporal scales, for example, following strong meteorological events such as Saharan dust storms or intense anthropogenic inputs.

Al Cd Co Cr

28–279 0.12–0.16 0.05–0.36 0.25–1.30

Atmospheric loads diluted within the surface mixed layer (a) 95–2850 0.41–1.63 0.17–3.67 0.85–13.3

Cu

1.86–3.56

6.32–36.3

89–133

4.8–40.8

Fe Hg Ni Pb Zn

6.4–384 0.01–0.03 1.1–2.6 2.5–5.2 77–165

22–3912 0.034–26.5 3.74–26.5 8.5–53.0 262–1683

14–112 0.1–0.4 135–299 16.6–35 111–216

20–28,023 8.5–260 1.3–19.6 24.3–319 121–1515

Range of seawaterTM labile atmospheric fluxes

1349 7.3–11.2 5.27 140

Impact of atmospheric fluxes on seawater concentrations (a/b) 7–211 3.6–22.3 3.2–69.6 0.6–9.5

Mean/range of dissolved marine concentrations (b)

Typical profile

Surface enriched Surface depleted Surface enriched Surface depleted Surface enriched/depleted Surface enriched Surface enriched* Surface depleted Surface enriched Surface enriched

Table 6.1. Mean seawater-labile atmospheric inputs (µg m−2 d−1), the same diluted 3 3 within the surface mixed layer (µg m− ), marine concentrations (µg m− ), impact of atmospheric loads on sea surface chemistry (%) and resulting typical profile. For details and original references, see Heimbürger et al. (2011). (*) Volatile Hg formation in the surface layer may alter this characteristic (see section 6.2.2)

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Since the residence time of TMs in open surface waters is shorter or equal to the renewal of deep waters, the vertical distribution of dissolved TMs in the LS and the surrounding marine regions depends on atmospheric fluxes; that is, during the stratification period, the atmospheric flux determines TM concentrations above the thermocline. 6.2.2. Mercury Mercury (Hg) has probably been the most studied chemical in the Med over the last 40 years, with hundreds of papers mainly dealing with Hg in the biota. The reason is that in the 1970s, elevated Hg concentrations were observed in certain pelagic fishes (e.g. [BER 77]). Since then, several review papers have dealt with this problem, and concluded that it is a multi-causal problem with biogeochemical and ecological factors (e.g. [CHO 18, COS 05]). We will focus here on the biogeochemical aspects of the Hg cycle, which may be at the origin of the enhanced bioavailability of Hg in the LS as well as in the rest of the W Med. According to Minganti et al. [MIN 93], Hg concentrations in the surface offshore waters of the LS were, in the 1990s, as low as 1.5 pmol L−1, but might reach 12.5 pM. However, Hg concentrations measured in the middle of the LS at the BOA station (Figure 6.1) in 1994 were < 1.0 pM [SIC 97]. More recently, Hg profiles in the water column of the LS were obtained between July 2007 and May 2009 at DYFAMED (station Dy, Figure 6.1). The results are shown in Figure 6.2, which do not indicate any trend within the various subsurface water masses (LIW, TDW, WIW and WMDW), and the concentration range is similar to that in the adjacent marine areas, namely the Tyrrhenian Sea (stations Tyr-1 and Tyr-9, Figure 6.1) and the Northern Current (station Antares, Figure 6.1), as well as in the entire NW Med [COS 18]. However, from Hg time-series measurements, fluctuating concentrations were noted in the MAW with some high values (up to 1.9 pmol L−1). Surface waters of the LS, as in the rest of the NW Med, are affected by the deposition of Hg conveyed by Hg-enriched air masses from Northern Europe, mainly as a result of coal combustion, caustic soda production, power plants, and cement and waste incineration. Moreover, Hg deposition is not a continuous phenomenon and is concentrated during rain events. Conversely, Hg depletion in surface waters (as shown in the Tyr-9 profile in Figure 6.2) can occasionally occur as a result of Hg evasion from the sea surface to the atmosphere: the production of elemental Hg, governed

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by photo-reduction (irradiance being highly elevated in the LS according to Cuny et al. [CUN 02]) and microbial reduction of divalent Hg, promotes Hg volatilization from the sea surface, a process well documented in the MAW of the W Med (e.g. [KOT 17]). These contrasting situations generate large variability in the Hg concentrations of surface and subsurface waters (Figure 6.2). The ratios of Hg concentration surface enrichment to deep-water concentration (Δc/c >> 1; Table 6.1) means that Hg is not removed from surface waters during their passage in the LS. We suggest that the Hg enrichment in surface waters is advected westwards, and may contribute to the slight Hg enrichment of the WIW and WMDW observed in the northern gyre off the Gulf of Lion [COS 18].

Figure 6.2. Mercury profiles in the water column (station Dy) and adjacent areas: stations Antares (March 2, 2011), Tyr-1 (October 27, 2004) and Tyr-9 (April 3, 2004). Dy-2 (September 1, 2007), Dy-3 (October 4, 2007), Dy-4 (November 14, 2007), Dy-11 (June 17, 2008), Dy-12 (July 7, 2008) and Dy-13 (September 21, 2008)

The sedimentary Hg profile determined at station Dy (Figure 6.1) helps to quantify the anthropogenic fraction of Hg in the LS. An enrichment was observed within the first 2 cm below the sediment–water interface (Figure 6.3a), which corresponds to sediments accumulated over the last approximately 60 years [HEI 12]. It is well known that Hg emissions in Europe dramatically increased over the 20th Century, accelerating after World War II and peaking at the end of the 1960s [HYL 03]. The Hg distribution at station Dy is partially consistent with this chronological

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scenario. The beginning of this increase indeed occurred 150–100 years ago; the recent expected decrease in deposition is only slightly indicated by a reduction in the rate of the Hg increase within the surficial sediment at 0.5 cm depth (Figure 6.3a). The occurrence of a smooth Hg profile may not reflect real-time variations of the inputs, as they may partially be the result of bioturbation. Elevated Hg concentrations in particles collected by sediment traps (20 m above sea floor) and in the uppermost sediment layer even suggest recent inputs of anthropogenically impacted material (Figure 6.3b and c), and the Hg and 206/207Pb relationship suggests a common atmospheric origin of Pb and Hg as a result of fossil fuel burning, most likely dominated by coal combustion [HEI 12]. With the hypothesis of the absence of significant post-depositional Hg redistribution, Hg enrichment from pre-industrial to present time is calculated to be approximately 60%. However, based on the chemical composition of the trapped material collected in sediment traps located 20 m above sea bottom, epibenthic mobilization of Hg, as organic carbon (Corg) is demineralized, could be significant (Figure 6.3b). More research is needed to clarify this issue. In particular, a possible biogeochemical rearrangement of Hg distribution at the sediment–water interface, as suggested by Gobeil et al. [GOB 99] for Arctic sediments, has to be considered. Inorganic Hg is the precursor for the production of methylated Hg (MeHg) in the open sea, which has been shown to be the main MeHg source in the NW Med margin [COS 09, COS 17]. These authors as well as others highlight the importance of organic carbon remineralization in the production of MeHg in the open ocean. In the LS, only one time series of high-resolution vertical profiles of MeHg in a pelagic environment is available: Heimbürger et al. [HEI 10a] showed that MeHg concentrations varied approximately 0.30 pM (SD = 0.17 pM for 214 determinations), with the lowest values at the surface, increasing with a depth up to the oxygen minimum zone and then decreasing slowly at a greater depth. The results of this study support the paradigm that Hg methylation in the open ocean occurs in the water column and is linked to organic matter regeneration. Mercury methylation is known to be encoded by a pair of genes present in prokaryotes [PAR 13]; however, recent results have suggested important roles for extracellular methylation mechanisms and demethylation in determining methylated Hg concentrations in marine oligotrophic waters [MUN 18].

Figure 6.3. (a) Mercury (Hg) profile in a sediment core of the Ligurian Sea (station Dy), and Hg relationships with (b) organic carbon (Corg) and (c) Pb stable isotopes

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In the following, the Hg pathway between its entrance from the atmosphere to its bioavailability to plankton (as MeHg) and subsequent biomagnification in food webs is summarized: – Hg entering the LS mainly via atmospheric deposition (about 1.3 kmol yr−1) is added to the Hg (about 38 kmol yr−1) conveyed by waters advected from the Tyrrhenian Sea and the Provençal Basin. A portion of this is incorporated into plankton, and the rest is released into the atmosphere or transferred to the sediment. – Hg (with about 0.2% as MeHg) is buried in the bottom sediments of the LS at a slow rate (about 30 mol yr−1); thus, the LS is not a location for high Hg accumulation in sediments. The Hg from the atmospheric source is probably predominantly reinjected into the atmosphere after its deposition, and another fraction is exported via the Northern Current, which contributes to the Hg enrichment of the WMDW. – Hg is transferred downwards into settling particles by the action of the biological pump in spring and the formation of dense water in winter, but Hg may accumulate in surface waters during stratified periods in summer and autumn. In this case, the downward transfer is postponed and occurs further west after horizontal advection within the Northern Current. – Once Hg has reached the low oxygen zone in the water column, inorganic Hg is methylated by microbial mediation. Further up and further down in the water column, MeHg is photochemically and biologically demethylated respectively. – Because Hg methylating layers (low oxygen zone) are relatively close to the surface (about 200 m) in the Med, the MeHg contact with Med epipelagic ecosystems is favored [COS 12], as shown thereafter in other environments: the Arctic [HEI 15] and Black Sea [ROS 18]. High-resolution MeHg profiles strongly suggest that sediments are not a significant source of this Hg species in the water column. This conclusion reinforces the role of the water column in the Hg contamination of the pelagic food web. As expected from the implementation of the Minamata Convention [MIN 17], Hg inputs to Med waters should decrease with a consequent progressive decrease of MeHg availability in the ecosystems. This decrease should be relatively rapid in the W Med as the residence time of waters is

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relatively short (decade scale). However, climate change, especially the possible increasing autumnal rain volume in the LS region [GAL 18], may increase the regional Hg deposition, whereas the increase in water temperature [RIC 19] should increase bacterial activity and the consequent Hg methylation rate by microorganisms [PAR 17]. Moreover, a temperature increase and proliferation of prokaryotes may accelerate oxygen depletion [ARÍ 05] and consequently favor the Hg methylation process [COS 13]. In this context, it is interesting to note that the LS is one of the Med regions where “bacterivory is the major pathway of organic carbon remineralization under oligotrophic and mesotrophic sub-surface conditions” [ZOC 16]. Indeed, this pathway may favor the efficiency of MeHg incorporation at the base of the Ligurian food chains. 6.2.3. Tributyltin (TBT) According to Mee and Fowler [MEE 91], TBT is the most toxic substance introduced into the marine environment; sublethal effects have been observed at levels as low as 1.7 pM. It was used as an antifouling compound on marine ships for more than 40 years [MAT 13], but was then banned in 2008. One of the few studies on TBT in an open-sea system was conducted in 1998 in LS waters. Surface concentrations ranged from 0.14 to 0.80 pM, which was consistent with the intense ship traffic in this region. The vertical TBT distribution in the water column (0.02–0.07 pM) suggests an important vertical transport with winter convection. TBT was also studied in NW Med coastal waters, with the highest concentrations found in the seawater of harbors (up to 0.8 nM), clearly as a result of ship activity and decreasing offshore with increasing distance from point sources [TOL 96]. A decreasing trend in TBT concentration in harbor water was recorded between samples taken in 1988 and 1995; however, for Fossi and Lauriano [FOS 08], the ecological risk is still persistent. Further changes in TBT contamination in the LS need to be studied in the context of the ban of this compound from ship hulls in 2008. The situation described for TBT in LS coastal waters is believed to be common to the entire W Med. Organic booster biocides and copper, the “new” antifouling agents now used instead of TBT, also need to be monitored in the marine environment where the ship traffic is as intense as in the LS.

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6.3. Radionuclides fluxes A variety of activities introduce radioactivity into the marine environment, for example military activities, nuclear fuel cycle operations, and radioisotopes usage by research centers, hospitals and industry. Nevertheless, the main sources of artificial radionuclides for the Med are the atmospheric fallout arising from past nuclear bomb testing and the Chernobyl accident (see Chapter 2), and the washout of river catchment basins contaminated by this fallout as well as from routine discharges from the nuclear industry. Atmospheric fallout is still a significant pathway for inputs onto land and into the ocean, but fission products in the stratosphere are constantly being reduced by radioactive decay. Thus, the present inputs of concern are intermediate (3H, 90Sr and 137Cs) and long-lived anthropogenic radionuclides (mainly plutonium isotopes). The Med received substantial amounts of fallout from the Chernobyl accident in late April 1986, but precise estimates of the total input are difficult to make because the deposition pattern was patchy and depended on plume trajectories. The radioactive contamination resulting from this accident was dominated by cesium isotopes and did not contribute substantially to plutonium inputs. Atmospheric fallout is mainly controlled by wet deposition, which removes more than 90% of radionuclides from the atmosphere. For example, Lee et al. [LEE 03] showed that the deposition of anthropogenic radionuclides over the NW Med basin mainly occurred during the spring and autumn, both seasons of heavy rainfall. However, they also reported that a substantial fraction of annual atmospheric radionuclide input entered via the periodic Saharan dust events, for example up to 29–37% for 137Cs and 34% for 239,240Pu. Aerosol measurements in France demonstrated a progressive decrease in 137Cs activities from 1959 to 2004, with present mean concentrations of 137Cs on the French Med coast being very low at 5 × 10−4 mBq m−3. However, the mean annual airborne 137Cs level at Toulon has not diminished since 2000, indicating that the 137Cs concentration in the atmosphere is mainly fed by soil resuspension processes such as wind erosion (e.g. Saharan dust) or wildfires [JOH 03]. 137

Cs is known to behave as a conservative radionuclide in marine waters because its distribution is mainly controlled by physical processes such as water mass advection and convection. In contrast, the distribution of

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plutonium nuclides is also governed by its chemical speciation and its strong binding with particles, which results in its more effective removal from the water column than 137Cs. Both radionuclides have decreased with time in Med surface waters [BRE 17, FOW 00]. In the case of 137Cs, it tends to increase with time in deep waters due to its conservative behavior. Papucci et al. [PAP 96] thus observed an increase from an average of 1 mBq L−1 below a depth of 1000 m from 1970 to 1982 to a mean value of 2 mBq L−1 during 1986–1992 in the W Med basin. In the case of 239,240Pu, Fowler et al. [FOW 00] reported a 62% decrease in concentrations in the surface waters of the NW Med between 1990 and 1999. Based on published 239,240Pu vertical flux data and measurements from the DYFAMED time-series station, a more recent analysis suggested that between 1989 and 2013, sinking particles accounted for a loss of 60–90% of the upper water column (0–200 m) 239,240 Pu inventory [BRE 17]. Earlier residence time estimates for plutonium in the W Med range from two to three years in the high sedimentation, for example the Lacaze-Duthiers canyon regime in the Gulf of Lion, to 15–30 years in the open NW Med waters [FOW 90b, PAP 96]. More recently, Bressac et al. [BRE 17] examined 239,240Pu water column inventories in the 0–200 m layer of the open NW Med waters. They found that seven separate inventories decreased exponentially from 8.1 ± 0.8 Bq m−2 in 1976 to 2.1 ± 0.2 Bq m−2 in 2013, with a best fit of the data giving an upper water column residence time of 28.5 years, a value which falls within the range of earlier estimates (20–30 years) for the 0–200 m layer at DYFAMED [FOW 00]. For the more particle-reactive transuranic nuclide, 241Am, it has a shorter residence time (5–10 years) in open NW Med surface waters, which is due to its greater binding affinity than plutonium for aluminosilicate particles that frequently enter these waters via Saharan inputs (ibid.). In 2001 and 2013, Bressac et al. [BRE 17] measured vertical profiles of the long-lived alpha-emitter 237Np from the surface to over 2000 m depth at the DYFAMED station in the open NW Med. Concentrations were generally low and similar ranging from 0.12 to 0.27 µBq L−1 for samples from both years. The observed overall similar geochemical behavior of 237Np and 137Cs in seawater indicated that 237Np behaves conservatively. Using the total integrated deposition of Chernobyl-derived 239,240Pu in Monaco (10 mBq m−2 [WHI 88]) and Np/Pu ratios in the reactor core, these authors estimated that the Chernobyl 237Np deposition in NW Med waters was approximately

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1 µBq m−2, roughly five orders of magnitude lower than that from global fallout, indicating that Chernobyl inputs of 237Np in this area of the Med were negligible. Concentrations of 137Cs and 239,240Pu have been detected in the deep sediments of various parts of the Med and are present in the uppermost centimeters of the sediment (e.g. [GAR 09]). Their concentrations and inventories in coastal environments are generally higher because, in certain locations, the contribution of land-based sources exceeds atmospheric inputs, for example near the Rhône River mouth or in the vicinity of Palomares in Spain [GAS 92]. Furthermore, in contrast to seawater, 137Cs has a high affinity for particles in fresh water, and part of the cesium that is strongly fixed in clay lattices does not desorb into seawater. This process, in addition to flocculation and aggregation near river mouths, has led to an accumulation of radionuclides in near-shore sediments drained by riverine systems. For the Rhône River, Charmasson [CHA 03] reported that the 137Cs inventory in the sediment over a 480 km2 prodelta area near the river mouth reached 19.6 TBq in 1990, which represented 40% of the total amount of 49 TBq stored over the entire 11,000 km2 watershed. Furthermore, it was calculated that at least 50% of this 137Cs originated from nuclear liquid released from various nuclear power plants and the Marcoule reprocessing plant situated upstream along the Rhône River. Measurements of anthropogenic radionuclides in marine organisms in the Med also highlight the continuing decrease in radionuclide levels due to corresponding temporal decreases in radionuclide inputs [CAT 06, PAP 96]. The most comprehensive data for any organism has been generated from radio-analyses of the mussel Mytilus galloprovincialis, an excellent bivalve bioindicator species which has been analyzed for the last three decades along the French Med coast. Some recent results from the 2004–2006 period have allowed a comprehensive mapping of 137Cs concentrations in mussels on a basin-wide scale [THÉ 08]. Levels are very low, less than 1.5 Bq kg−1 fresh weight, and the study has clearly shown the higher residual contamination from the Chernobyl accident in the Black Sea compared to that in the NW Med and other basins. In comparison, little work has been done to examine the trophic transfers of artificial radionuclides in the NW Med basin. At lower planktonic trophic levels, very little plutonium ingested by crustacean zooplankton is assimilated, and Pu does not bioamplify between prey and predators. Higgo

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et al. [HIG 77], when analyzing plankton from NW Med waters, found that 239+240 Pu concentrations in the euphausiid (Meganyctiphanes norvegica) were one order of magnitude lower than the corresponding concentrations in their microplankton prey. Furthermore, they showed that the majority of the ingested plutonium is not assimilated into the organism’s tissues, but is excreted in plutonium-rich fecal pellets that contribute greatly to the downward vertical transport of this radionuclide in these waters and elsewhere. The importance of upper water column biological mechanisms in distributing atmospherically derived radioactivity in NW Med waters was highlighted by sediment trap experiments carried out just before and after the Chernobyl accident. Time-series sediment traps moored off Corsica in April–May 1986 demonstrated that the maximum concentrations of 137Cs, 239+240 Pu and 241Am in sinking particles were noted as a pulse passing 200 m depth roughly one week after the maximum radionuclide atmospheric deposition reached the surface waters of the LS around May 4 [FOW 87, WHI 88]. In the case of 239+240Pu, the integrated vertical flux through May 21 was calculated to be 7.5 mBq m−2, which suggested that approximately 75% of the amount deposited on the sea surface had fluxed through 200 m depth within one month following the accident. Furthermore, these particle flux experiments clearly demonstrated that sinking fecal pellets excreted by zooplankton were largely responsible for the rapid removal of the Chernobyl fission products and transuranic radionuclides to 200 m depth in a matter of a few days (see Chapter 2). In contrast to Pu, recent studies that examined the 137Cs content in the muscle of hake (Merluccius merluccius) and their prey in the Gulf of Lion have shown an increase in the 137Cs concentration with hake size, with males generally having higher concentrations than females [HAR 12]. Furthermore, using δ15N measurements as a proxy for the trophic level, the content of 137Cs in hake relative to that in their prey has also shown a tendency to increase with the trophic level, which has been considered as evidence for biomagnification in this segment of the hake food chain. Nevertheless, the increase in 137Cs biomagnification between prey and hake remains less than a factor of 5. It is expected that the general trend for decreasing inventories of the anthropogenic radionuclides 137Cs, 237Np and 239+240Pu will continue in the NW Med due to the present absence of relevant input sources, the natural

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physical water circulation, biogeochemical processes occurring in the water column and sediments, and in the case of 137Cs through radioactive decay. Although the authorized releases from nuclear power plants do not lead to significant amounts of contamination in these waters, potential accidents in European and nearby nuclear industries could result in future inputs of radionuclides to the Med. In addition, climatic changes that may cause increases in the frequency and intensity of wildfires and wind erosion around the Med basin could release soil-bound radionuclides over short time scales, thus contributing to the present levels, particularly those of 137Cs, in the atmosphere as well as potential fallout for Med waters. The database for these long-lived anthropogenic radionuclides, which has been built over the past four decades in the NW Med, can serve as a solid baseline for future radionuclide monitoring in this region. 6.4. Organic chemical contaminants The Mermex Group [THE 11] has reviewed the state of contamination of the W Med by organic chemical contaminants (OCCs), including polycyclic aromatic hydrocarbons (PAHs), polychlorobiphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), perfluorochemicals (perflurooctane sulfonates (PFOS) and perfluorooctanoic acid (PFOA)), alkylphenolic compounds (nonyl- and octylphenol), many pesticides and phenyl urea herbicides, and veterinary and human pharmaceuticals, biocides, bactericides and finally phthalate esters. Unfortunately, we are obliged to note that biogeochemical studies of most of these OCCs in the waters of the LS are sparse, except for substantial baseline information on PCBs and PAHs. In the mid-1970s, the interest was focused on testing the hypothesis that sinking particles were responsible for the presence of anthropogenic contaminants such as long-lived radionuclides and PCB compounds in deep-sea sediments and benthic organisms. Zooplankton in the upper water column were proposed as probable vectors for affecting such a mechanism through their grazing activities by producing fast sinking fecal pellets and other detritus that could scavenge and transport contaminants to depth. To test this hypothesis, zooplankton, primarily the euphausiid Meganyctiphanes norvegica (see Chapter 4), were collected at night while feeding in the surface layers off Villefranche-sur-Mer and immediately transferred to onboard and large-volume fecal pellet collectors which were used to separate

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the excreted fecal pellets from the organisms producing them [LAR 76]. The pure samples of fecal pellets were subsequently prepared in the laboratory and analyzed for PCB compounds. PCB (as DP-5) levels in four separate collections of euphausiid fecal pellets ranged from 4.8 to 38 µg g−1 dry weight (dw) with an average value of 17.5 µg g−1 dw [ELD 77]. These concentrations on a wet weight basis were approximately 1 × 106 higher than the corresponding concentration present in the surrounding water. Furthermore, the concentrations in feces were approximately 4–21 times higher than the levels in the microplankton food that formed the fecal pellets, suggesting a concentrating process via ingestion and digestion of the PCB-contaminated microplankton. While such analytical evidence strongly supported the hypothesis that zooplankton defecation leads to the rapid transport of PCBs to depth, the downward vertical flux of particulate PCBs needed to be quantified to verify the hypothesis. To do this, the first sediment trap deployments took place from June to October 1978 off the coast of Monaco. Based on measured particulate mass fluxes (0.40–0.77 g m−2 d−1, dw) and PCB concentrations in the sinking particles (200–710 µg kg−1 dw), the first quantitative data on particulate PCB deposition fluxes ranged from 150 to 500 ng m−2 d−1 (56–183 µg PCB m−2 yr−1). These sediment trap measurements agreed closely with an independent estimate of PCB deposition fluxes (80–125 µg m−2 yr−1) based on PCB levels measured in bottom sediments from the same coastal area where the traps were moored [FOW 79]. In contrast, they were significantly higher than particulate PCB fluxes (6.9–24.9 ng m−2 d−1) measured in the Alboran Sea some 14 years later [DAC 96]. Despite these different locations in the W Med, the large discrepancy in flux could reflect an overall reduction in PCB usage and inputs during that 14-year period. It was also noted in the Monaco sediment trap samples that intact fecal pellets represented approximately 10% of the total particulate matter (dw). Freshly produced pellets from copepods placed in the pellet collectors contained approximately 1,300 µg PCB kg−1 dw, a level lower than that measured previously in the larger euphausiid pellets. The relatively high levels of PCBs in both sinking fecal matter collected in situ in sediment traps and the high concentrations in freshly produced fecal pellets from copepods residing in the same waters have clearly demonstrated that zooplankton defecation significantly contributes to the downward flux of these contaminants. With the sinking speeds of copepod fecal pellets being

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typically about 50–150 m d−1, these particles have the potential to reach the bottom in most coastal areas of the LS. Polycyclic aromatic hydrocarbons (PAHs) are both natural and anthropogenic compounds found in coal and oil deposits, and also produced by the thermal decomposition of organic matter. At the end of the 20th Century, the sum of PAH concentrations (ΣPAHs) in Med aerosols ranged from 0.2 to 2 ng m−3 [LIP 97], whereas the total deposition of ΣPAHs, estimated by the same authors from Balearic Sea samples, ranged from 0.11 to 0.23 µg m−2 d−1. Particulate PAH fluxes across the LS water column were calculated from two sediment trap samples (200 and 1000 m). In the LS, the ΣPAH fluxes ranged from 0.30 to 0.91 µg m−2 d−1 during a short period in 1987 [LIP 93], and varied over a wider range for a longer period during 2000–2002 (0.04–4.74 µg m−2 d−1), testifying to large seasonal and interannual variations. The distribution of PAHs and ratios of specific compounds in sediment traps showed a marked contamination in petrogenic hydrocarbons, whereas pyrolytic hydrocarbons were in the range of those in other open Med locations [DEY 11]. According to the same authors, sinking hydrocarbons were efficiently transported from 200 to 1000 m depth. A sediment core, collected at DYFAMED (station Dy, Figure 6.1) during the “Envar-4” cruise of the R/V Suroît in 2006, was analyzed for the distribution of PAHs at three different depths below the water–sediment interface, namely at intervals of 0–0.5, 0.5–1.0 and 1.0–1.5 cm. Parent compounds are commonly associated with biomass and fossil fuel combustion. Alkylated compounds have frequently been used as tracers of crude oil. The distribution of alkylated and parent PAHs and depth profiles of selected individual molecules are shown in Figure 6.4. Both categories show similar profiles with depth in the sediments, suggesting recent and still increasing contamination since the top 1.5 cm of sediment is younger than 40 years [HEI 12]. The PAH contamination of the LS sediment seems to originate mainly from combustion processes. The anthracene-to-(anthracene + phenanthrene) ratio of 0.14–0.16 suggests the dominance of pyrogenic sources [BUD 97], whereas the indenopyrene-to-(indeno)pyrene + benzo(ghi)perylene ratio is approximately 0.44, a value close to ratios reported for coal combustion [YUN 02]. In brief, the PAH contamination of the LS is significant and originates from both petrogenic and pyrolytic sources, but pyrolytic PAHs seem to be better preserved in the sediment (Figure 6.4).

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Figure 6.4. Polyaromatic hydrocarbon (PAH) distributions in deposited sediments and sediment trap at station Dy in the Ligurian Sea

Except for the previous examples, little documentation is available specifically about OCCs in open LS waters. The few existing papers concern persistent organic pollutants (POPs) accumulated in the tissues of marine mammals. For example, striped dolphin blubber showed high PCB and dichlorodiphenyltrichloroethane (DDT) concentrations (50 and 30 µg g−1 dw

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respectively) with, in contrast, a decreasing trend of 30% between 1993 and 2007 [FOS 13]. Fin whales also contained similar concentrations of these two compounds. According to the same authors, these values were higher than those in dolphins from the Tyrrhenian Sea, probably a result from the greater industrialization and abundance of agricultural activities around the LS. In addition, PBDEs, PCDDs and PCDFs were found in the liver of striped dolphins from the LS (e.g. [MAR 18]). As observed for PCBs, the transport of POPs to the ocean is mainly governed by the efficiency of the atmospheric net deposition and the marine cycle of organic carbon. Primary production and settling particles shift the partition of POPs between surface waters, deep waters and sediments. Thus, it can be inferred that climate changes may affect the fate of OCCs in Med waters. While an increase in primary production and efficiency of the biological pump could strengthen the air–sea exchange and their incorporation into sediments, the oligotrophication of waters would favor an increase of OCC stocks in the atmospheric gaseous and marine dissolved phases. For emerging OCCs, the Mermex Group [THE 11] concludes that: “Better knowledge of the distribution, partition, and speciation of the emerging organic contaminants (including more hydrophilic compounds) is required in order to predict their fate, mainly on the basis of changes in their degradation rates (microbiological and photochemical), and to assess the resulting risk for the different ecosystems.” This is definitely an important area for future research, especially in the LS. 6.5. Contamination of the LS in the context of the global change Global change refers to planetary-scale changes in the Earth system, and the LS is not immune to these changes. Climatic changes are probably the most urgent and demanding challenges we are facing, but global change also includes other critical issues, in particular changes in the rate of anthropogenic emissions. As TMs are emitted from land-based sources and mostly transported by the atmospheric pathway to open waters, trends in marine concentrations of metallic contaminants should be primarily considered in the atmospheric compartment. Decadal trends cannot be assessed without observations

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spanning over a minimum duration of 20 years. To our knowledge, the only land-based time-series station in the NW Med of this format is the Cap Ferrat station, located on the SE coast of France, which is part of the time-series stations in the framework of the Mediterranean Ocean Observing System of the Environment [MIG 15, MOO 15], the characteristics of which have been detailed in several papers (e.g. [HEI 10b]). This site is protected from direct contamination, and it is supposedly representative of the chemical composition of the Ligurian troposphere [SAN 97]. The most recent study on decadal shifts in atmospheric aerosol fluxes was carried out by Heimbürger et al. [HEI 10b]. From observations between 1986 and 2009, these authors distinguished three groups of TMs: crust-derived TMs such as Al, Fe, Mn and Co; anthropogenic TMs such as Pb, Cd and Zn; and intermediate TMs, i.e. metals that are of both anthropogenic and natural origins such as Ni and Cu. Airborne concentrations of crustal TMs did not show clear changes during the sampling period, but potential changes might be masked by the strong interannual variability characteristic of these pulsed inputs. In contrast, the concentrations of anthropogenic TMs decreased significantly. Pb is a well-known example (from approximately 30 ng m−3 on average in 1986 to approximately 3 ng m−3 in 2008, i.e. a 90% decrease owing to the widespread phasing out of leaded gasoline). Cadmium and Zn concentrations decreased by 66 and 54%, i.e. from 0.27 to 0.09 ng m−3 and 23.9 to 10.9 ng m−3 respectively. Nickel and Cu concentrations remained constant overall. Figure 6.5 shows the changes in concentrations recorded for Pb, Cd and Zn in the NW Med water column for the same period (1983–2013). A clear decrease was recorded for Pb, especially in surface waters (Figure 6.5a), as reported by Nicolas et al. [NIC 94] and later by Migon and Nicolas [MIG 98] for the period 1983–1995, whereas Cd and Zn concentrations failed to show any significant trend in the last three decades (Figure 6.5b and c). The deposited sediments (station Dy, Figure 6.1) also revealed anthropogenic contamination by Pb and Zn (as well as by Hg, Figure 6.3) that affected the first centimeters below the sediment–water interface, i.e. the sediment deposited since the start of the Industrial Revolution 170 years ago [HEI 12]. Conversely, no clear temporal change was observed in the Cd deposition profile.

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Figure 6.5. Temporal trends in anthropogenic trace metals (Pb, Cd and Zn) in the waters of the W Med since 1983

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Decadal trends of TMs, such as Pb, Zn and Hg, emitted in large amounts by anthropogenic activities, seem to be sensitive to antipollution policies, the implementation of which is the key factor to actually determine a rapid environmental response. The evolution of crustal/natural TMs is presumably dependent on the climate and meteorology, but the indirect effects of global change on their concentrations in the atmospheric aerosol, water column or sediment have not yet been observed. This last point should be an interesting avenue for future research. In the case of the anthropogenic radionuclides 137Cs, 237Np and 239+240Pu, their inventories will continue to decrease in the LS due to reduced input sources, radioactive decay, water circulation patterns and biogeochemical processes that occur in water and sediments. The only possible significant future inputs in the Med would arise from potential nuclear accidents in European and neighboring countries, or from climatic changes that would cause increases in the occurrence of wildfires, strong wind and rain erosion that could release soil-bound radionuclides into the atmosphere, thus enhancing fallout into LS waters. It may be supposed that the offshore fluxes of OCCs follow the time trend observed during a Mussel Watch program on the seashore of the French coast, where, for example, PCBs and dioxin concentrations have tended to decrease in the last 20 years [MUN 08]. Anthropogenic emissions for other contaminants need to be better documented, in order to estimate the resulting trends in the atmosphere and seawater. Among the expected modifications in the Med environment due to global change, we can mention: a significant seawater warming, increased acidification, hypoxia development, decrease (or local increase) in precipitation, changes in the thermohaline circulation with an increase in vertical stratification, reduction of net phytoplankton productivity and changes in the food chain structure [RIC 19]. Seawater warming means a possible increase in microbiological activity, including remineralization rates of particulate organic matter with subsequent redissolution of certain TMs and anthropogenic radionuclides, and an increase in biomediated reactions such as methylation/demethylation or redox reaction of inorganic Hg with the formation of dissolved gaseous

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Hg. Hypoxia development would favor anaerobic prokaryotes, many of which are potential Hg methylators. In contrast, Hg reduction and MeHg demethylation, which are mainly governed by photochemistry, would be affected by an increase in UV radiation. An increase in MeHg demethylation and subsequent Hg volatilization from the sea surface would engender an increase in Hg deposition around the periphery of the Med, enhanced by a local increase in autumnal precipitation in the LS. Conversely, a regional decrease in rain volumes would mean less deposition of volatile contaminants, including OCCs and TMs. Acidification would favor the decomposition of gaseous dimethylmercury into mono-methylmercury, thereby increasing the bioaccumulation potential of Hg. In the case of particle-associated radionuclides such as plutonium and americium, acidification may lead to dissolution and release into the water column, resulting in their increased bioavailability in marine food webs. Increasing vertical stratification will cause major changes in the vertical flux of contaminants through the water column, and most likely enhance MeHg production at the subsurface pycnocline. As recently modeled by Kessouri et al. [KES 18], two mixing regimes exist in the LS (as well as in the majority of the NW Med), i.e. deep and shallow convection regimes (see also Box 6.1). However, under the influence of an increase in water column stratification, the SE Med regime could develop, with the consequence of reducing the efficiency of contaminant transfer to the bottom sediments, and their corollary increase of the lateral advection ultimately reaching the adjacent NE Atlantic Ocean. A possible decrease in plankton productivity may slow down the uptake and subsequent scavenging and vertical transfer of most of the hydrophobic organic contaminants and plankton-sorbed TMs and anthropogenic radionuclides. Changes in the structure of the food web will inevitably change the bioaccumulation patterns of biomagnifiable contaminants (e.g. organohalogens and Hg) according to the processes already discussed in the case of the Med (e.g. [CHO 18]). In this context, research efforts should be geared towards studies of accumulation processes of chemical contaminants, especially at the base of food webs (i.e. where the bioaccumulation factors are the highest), namely the bioconcentration step from seawater into phytoplankton and subsequent assimilation in various trophic regimes, especially those in the LS.

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Knowing which parameter controls the removal of organic carbon and chemicals, including contaminants, from surface waters to the sea bottom has been a matter of debate over the last two decades (e.g. [PAS 04]). Dissolved matter is transferred to depths via its assimilation by phytoplanktonic organisms. Early studies (e.g. [FOW 87]) have suggested that the removal of suspended particles in the surface layer (essentially of atmospheric origin in offshore areas) is governed by biological activity, i.e. adsorption onto phytoplanktonic debris and packaging within fecal pellets. Indeed, the settling velocity of individual atmospherically deposited particles (< 1 m d−1) is believed to be negligible, which agrees with Stokesian settling calculations [STO 01]. Other studies have pointed out the prominent role of the process of dense water formation and the subsequent vertical mixing in the magnitude of export fluxes (e.g. [MIG 02]). Some authors have suggested that mineral particles, originating mainly from atmospheric dust deposition, and biogenic minerals (carbonates, silica) control the downward transfer of matter (e.g. [ARM 02]). However, Heimbürger et al. [HEI 14] observed from Ligurian particle trap data (DYFAMED site) a highly significant correlation between the concentrations of a variety of metals, regardless of their nature, emission source and depositional pattern. In addition, atmospheric and marine fluxes do not exhibit the same temporal variability. This observation is confirmed by the fact that some significant Saharan dust events, most likely to supply loads of mineral matter, did not result in a concomitant vertical export flux. At the present time, the most likely scenario of seasonal transfer of particulate contaminants in the Ligurian Sea would be the following: – In winter, the formation of dense water yields the rapid downward transfer of dissolved and particulate matter accumulated in the surface layer (“flushdown effect”). The driving force of the transfer is hydrology. It is worth noting that the efficiency of this transfer depends on external conditions (see Volume 1, Chapter 3 of this book series). – In spring, nutrients brought into the photic layer by convection permit early plankton blooms. The transfer is driven by biological activity. The intensity and quality of this activity strongly depends on the intensity of convection processes [HEI 13]. – In summer and autumn, the water column is stratified. Marine fluxes are very low due to the absence of hydrological or biological driving forces, and insignificantly account for the transfer of particles to depths. Atmospheric material accumulates in the surface layer, waiting for the next convection episode. Box 6.1. Vertical transfer of chemical contaminants

6.6. Acknowledgments Thanks are due to J. Tronczynski (Ifremer) for providing the results of HAP analyses of the sediment from Dy station.

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Conclusion and Perspectives

The observation, after nearly a century of studies of the Ligurian Sea, is that our understanding of how it functions has improved in proportion to the measures acquired in all fields. It is interesting to note that the statistical methods developed in the 1970s by Ibanez [IBA 73, IBA 80] sought to fill the gap in data acquired sporadically or on the simple path of an oceanographic vessel (sampling strategy), while those currently under development (machine learning) seek more to exploit the high frequency and diversity of acquired measurements. It is clear that the efforts to be made in the coming decades will focus on AI (Artificial Intelligence) methods capable of processing the volume, diversity and heterogeneity of data which is currently growing exponentially. This shift, initiated in the 1980s with the advent of satellite data, has continued since the 2000s with the technological revolution of autonomous vehicles (gliders, profiling floats) capable of transmitting, in real time and from any ocean location, vertical profiles of physical data (Argo program) and, more recently, biogeochemical profiles (BGC-Argo program). In the Mediterranean, the implementation on the Almeria–Oran front of SHET (Towed HydroElectric System – THES) was a precursor in this field, one of the first devices capable of revealing the complexity of mesoscale structures by measuring biogeochemical proxies along continuous transects [PRI 93]. Hydrographic structures have been observed off Villefranche-sur-Mer in the 1960s by Gostan and collaborators with the ships Winnaretta Singer and Job Ha Zelian, but the low resolution of 10–15 miles adopted at this time during their expeditions did not allow them to realize that they had unknowingly discovered the Liguro-Provençal front. Chapter written by Hervé CLAUSTRE, Lionel GUIDI and Antoine SCIANDRA. The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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One of the major challenges facing us today is therefore not only the intelligent processing of data from different categories of physico-chemical, optical and -omic (metabarcoding, metagenomic, metatranscriptomic, proteomic, metabolomic, etc.) data, which are becoming more frequent and widespread, but also the processing of their relationships. What will the next tools be, to reconcile the synopticity of satellite surface coverage with the scattering of vertical continuous profiles of autonomous platforms, and to achieve an even more accurate three-dimensional tomographic vision of the oceans?

Figure C.1. Time and horizontal space plot indicating a variety of ocean processes (a) along with rough coverage domains of various oceanographic platforms (b). The arrow on the figure are intended to draw attention to the cascade of energy and information from large to small scales as well as from small to large scales. From [DIC 05]

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“The first century of modern oceanography was a century of undersampling”, as stated by Walter Munk in 2010. This observation, which applied to physical measurements, is even more obvious for chemical and biological observations. Under-sampling, which has long been the rule, has significantly hampered our ability to understand and quantify many key biogeochemical processes, as well as their dependence on physical forcings. Indeed, since these processes occur on a continuum of spatial and temporal scales (Figure C.1), much of ocean variability has always escaped the broad mesh sampling traditionally carried out by oceanographic vessels. C.1. Latest developments in observation methods The last three decades have seen an unprecedented change in this. Satellite observations have been developed and diversified for a variety of physical (SST, salinity, altimetry) or biological (water color) properties of the surface ocean. These synoptic measurements, now systematic and sustainable, are called “operational” because they provide long-time series for the entire ocean. This is an essential step, not only to rigorously assess the impact of global changes on the biogeochemical properties of the ocean, but also to address and observe new scales of functioning (e.g. the interannual scale in phytoplankton biomass cycles [MAY 16]). The Copernicus Programme coordinates this long-term operational observation in Europe whereby the Mediterranean and, in particular, the Ligurian Sea are covered by these measures. In addition to satellite measurements, observation has benefited over the past 20 years from major technological and methodological developments implemented in situ. This progress is based primarily on the diversification of observation platforms. Thus, after the instrumented anchorages allowing fixed-point acquisition of long-time series of bio-optical (Compass) and biogeochemical (DYFAMED) measurements, underwater gliders and profiling floats were introduced. These autonomous platforms move by modifying their buoyancy. The profiling floats (Figure C.2) can take vertical profiles of various measurements between 2,000 m and the surface for six years, generally every 10 days, and then drift horizontally to a fixed depth the rest of the time. The underwater gliders (Figure C.3), piloted by an operator, carry out transects of several hundred kilometers over periods of up to six months. These autonomous platforms have been gradually equipped with new sensors, which now include physical (salinity, temperature) and

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then biogeochemical (oxygen, Chl a) measurements. These instruments are increasingly smaller in size and consume less power. This robot-sensor synergy, by providing an exceptional density of observations in the water column, has made it possible to fill the observational gaps identified by Walter Munk in 2010, particularly at the operating scales, the study of which had hitherto been impossible with conventional oceanographic campaigns.

Figure C.2. The PROVOR CTS-4 free-drifting profiling float equipped with (A) Iridium antenna; (B) oxygen sensor; (C) sensor for chlorophyll fluorescence, chromophoric dissolved organic matter (CDOM) fluorescence, and particle light backscattering at 700 nm; (D) nitrate sensor; (E) conductivity–temperature–depth sensor; (F) radiometer (3 Ed(λ), 1 PAR). From Organelli et al. [ORG 16], © American Meteorological Society. Used with permission

The Ligurian Sea was the testing ground for prototypes of underwater gliders equipped with biogeochemical sensors. The first radial, crossing the North Current at the end of winter, described, with unprecedented precision, the impact of geostrophic circulation to sub-mesoscale circulation on the nutrient enrichment of the surface layers, their use for primary production, and the subsequent transfer of this production to the mesopelagic zone [NIE 08]. More recently, the joint implementation of all-season radials and

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profiling floats at the DYFAMED–BOUSSOLE site has made it very clear that the center of the Ligurian Sea is, at the summer solstice, the site of very significant developments in chlorophyll maxima and particulate carbon. An example of conceptualizing the relationships between observations revealed by robots has been proposed by Mignot et al. [MIG 14].

Figure C.3. Deployment in the Ligurian Sea of the SeaExplorer SEA002 (LOV) submarine glider equipped with a 6th generation marine video profiter (UVP6)

C.2. Future evolution of observation techniques However spectacular they may be, these latest technological advances are only the first steps towards a future revolution in our methodology. Indeed, the expected progress will allow exploration with gliders and floats approaching the abyssal depths (6,000 m). New surface drones, such as “wavegliders”, will take advantage of the attenuation of wave energy with depth [DAN 11]. Autonomous sailing boats [MOR 17] with pre-programmed missions can be controlled with artificial intelligence. These surface units are used to acquire meteorological, oceanic (surface Chl a, gas exchanges at the air–sea interface) and acoustic (deep mesopelagic biomass) measurements. In addition, aerial drones make it possible to map the color of the water with a high spatial and spectral resolution, to appreciate all the nuances of its composition. The development of sensor technology necessarily accompanies that of vehicles. Relatively simple measurements of chlorophyll fluorescence or oxygen were followed by those of nitrates and pH, which are now routinely and permanently embedded on floats and gliders [JOH 17]. Miniaturized

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cameras are being integrated on these platforms, and the first tests carried out in the Ligurian Sea have already documented particle size distribution down to 2,000 m deep, soon to 6,000 m deep. These sensors will soon benefit from onboard intelligence to identify and quantify, in real time, the biomass associated with large zooplankton groups. Passive acoustic sensors for wind, rain, anthropogenic noise and marine mammal sound signatures are also being integrated into these platforms (e.g. [YAN 15]). “Off-the-shelf” turbulence sensors are candidates for integration on floats or gliders and may estimate, in the future, turbulent nutrient flows in the surface ocean layers. Other sensors for silicates, phosphates (the main limiting nutrient in the Mediterranean) and CO2 partial pressure sensors are currently under development. In parallel with these robotic and sensor developments, High-Throughput Sequencing (HTS) has become affordable, providing an unprecedented flow of metagenomic data (i.e. all data related to the genomes, transcriptomes, proteomes and metabolomes found in the environment or in a specific biological sample). Some examples of large sequencing projects include meta-HIT (Metagenomic of Human Intestinal Tract) [QIN 10], the Earth Microbiome [GIL 14] or Tara Oceans [KAR 11]. This latter sequencing revealed approximately 40 million genes, the vast majority of which are new to science, thus hinting towards a much broader biodiversity of plankton (from viruses to eukaryotes) than previously known [BRU 15]. Thanks to novel computer science methods, these data can help to predict how these diverse planktonic organisms interact [LIM 15]. Taken together, these resources give insight into how genes can inform on globally relevant biogeochemical processes [GUI 16]. Indeed, the relative abundance of a small number of bacterial and viral genes could predict a significant proportion of variations in carbon fluxes from the upper layers of the ocean to the deep ocean. However, the functions of most of these genes are still unknown. Understanding the structure of these networks of species and genes linked to the biogeochemistry of the ocean and our planet opens up a wide range of possibilities, especially for modeling the Earth system. Imaging technologies have revolutionized the view of particles and zooplankton in the ocean as fluorometers and ocean color remote sensing did for chlorophyll a few decades ago. For example, the use of imaging instrument such as the Underwater Vision Profiler (UVP) [PIC 10]

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characterized zooplankton, particle size distribution and the resultant carbon fluxes spatial distribution in the Mediterranean Sea. In the Gulf of Lion, UVP data combined with net samples allowed us to establish the impacts of deep water convection on the biology, suggesting an enhancement of energy transfer to higher trophic levels and organic matter export in the area [DON 17]. Similarly, UVP combined with LISST-Deep data provided evidence of the formation of the sea bed thick nepheloid layer composed of aggregates between 100 and 1,000 µm in diameter, which is coincident with deep sediment resuspension induced by the same events over a six year (2009–2015) long period [DUR 17]. Finally, consistent deployments of the UVP in the Mediterranean Sea, combined with drifting sediment trap data over the last two decades, have allowed the first assessment of carbon export at the basin scale level [RAM 16]. All of the above examples show the great potential of coupling advanced imaging and optical methods with more “traditional” techniques, to better understand the tight coupling between physical and biological mechanisms in the Mediterranean Sea. As presented above, observations (satellite and autonomous platforms) offer potential for a rough global coverage of key biological/biogeochemical ocean properties. On the other hand, high-level information (HTS and imaging), such as species relative abundance or metabolic activities, provides local but fine information on the biology of the ocean. These two different sets of ocean observations are, however, slowly coming together, as today ecogenomic and imaging sensors are becoming integrated on autonomous platforms (i.e. ESP, Table 1 in [OTT 16]), and gene distribution starts to be predicted from space [LAR 14]. Overall, HTS, imaging and remote sensing data provide massive heterogeneous data that challenges integration. However, in order to investigate ocean systems as a whole, we will have to merge quantitative measurements from physical sciences and imaging observations, to semi-quantitative observations from biology (meta-omics) into a single model. As a natural attempt, graphs are usually considered as a formal abstraction that can link this knowledge into a unique paradigm. However, application of graph-based integrative and comparative techniques to ocean systems is still in its infancy, and dedicated methods, inspired from distributed systems, language processing or data sciences, must be further investigated in the light of specific oceanographic questions.

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C.3. A growing contribution of methods based on artificial intelligence To accompany the considerable influx of new measures, learning methods are being developed. One obvious use of these approaches is the automatic taxonomic annotation of imaging data. These methods have dramatically increased the speed of sorting images into categories, even though validation by experts is still required [LUO 18]. In addition, AI methods can estimate variables of biogeochemical interest, for which automated measurement is still impossible or far too expensive. Their principle is based on the use of qualified mixed databases (e.g. [OLS 16]), i.e. containing variables measured with high precision by robots (e.g. Oxygen, Temperature, Salinity) and variables that are currently impossible to acquire with these same robots, but which are acquired with research vessels (e.g. silicates, phosphates, pCO2). Ad hoc neural networks applied to these databases can extract highly nonlinear empirical relationships between all these variables [BIT 18, ELH 19, SAU 17]. Applied to robotic measurement series, these relationships allow estimation, with very good approximation, of the variables of interest which are not measured or not measurable. These new approaches currently represent a growing field of research in the oceanographic community, because, by complementing the acquired fields of observation with predicted fields, they offer the advantage of making available, for a given geolocation and date, an increasingly exhaustive corpus of multidisciplinary measurements. This effort is an essential step in strengthening synergy with the modeling community, particularly operational modeling, as these new types of databases (acquired and predicted) are essential to initialize and validate models. As neural networks have been specifically developed for the Mediterranean, such databases will soon also be developed for this region, in line with those that now exist for the global ocean. Furthermore, AI techniques make data from different sources interoperable, such as the biogeochemical properties that ocean color satellites and floats measure, on the surface and vertically, respectively. The obvious complementarity between the two types of observation is enhanced by the emergence of new three-dimensional products, as has already been proposed at the global scale for particle backscattering, a proxy for particulate organic carbon [SAU 16]. In the long term, and thanks to

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a refinement of techniques and a densification of observations, these three- and four-dimensional reconstructions (over time) can be extended to new products (biomass and phytoplankton functional groups) or adapted to new spatial areas (e.g. the Mediterranean basin). Finally, it is worth noting the emergence of applications resulting from these new methods, through developments that seek to establish a phenomenological interpretation of the relationships that exist between the different variables [REI 19]. Thus, these artificial intelligence techniques, used until now as “black boxes”, could gradually form the basis for research more oriented towards understanding these relationships, in addition to the more traditional approaches to analytical modeling. However, these latest advances in robotics or methods of analyzing large databases should not deter future generations from continuing to use the more traditional means of investigation, which we will still need for a long time to come. Indeed, nothing will replace the experience of being in direct contact with the object of study, whether it is the ocean or the organisms that inhabit it. Because oceanography cannot be purely descriptive, the use of oceanographic vessels remains an absolute necessity to conduct process studies that are essential for understanding the intimate functioning of marine ecosystems and predicting their future evolution. Even though operations at sea are relatively complex and more expensive to carry out than the deployment of autonomous floats, future generations of oceanographers will benefit from investing part of their activity in setting up multidisciplinary expeditions that provide a favorable context for studying a system as complex as the ocean. Moreover, the synergy provided by the joint use of autonomous platforms and oceanographic vessels will be a considerable asset for future in situ studies. In this respect, the mesopelagic zone, intermediate between the surface zone that fixes atmospheric carbon and the abyssal zone that sequesters it, is home to species and processes that are still largely unknown, despite their supposedly essential role with regard to the various pumps that modulate carbon sequestration. Just as it is still necessary to “see” the ocean up close, it is also essential to continue to observe plankton organisms with precision. Although the progress made over the past decade in imaging, shape recognition, learning and genomics has made it possible, thanks, in particular, to artificial

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intelligence, to understand biogeochemistry and ocean biodiversity from a new angle, it does not allow for understanding the specific functioning of each type of organism, which still requires the use of appropriate breeding and observation techniques (microscopes). Can we really claim to know the ocean and how it works when we are still unable to maintain most of its component organisms in the laboratory (e.g. the way radiolarians feed)? C.4. Future themes requiring observation in the Ligurian Sea

integrated

and

multi-tool

Regardless of the object of observation or the scientific problem associated with it, the Ligurian Sea is a unique natural laboratory: – From the point of view of the seasonality of physical forcing, in a few months we move from one of the most intense and deepest examples of vertical mixing in the global ocean (similar to the North Atlantic sub-polar eddies) to relatively severe stratification conditions at the end of summer. This cycle is structuring in several respects: for the dynamics of phytoplankton biomass [BAR 19], for the developing ecosystem and for the export of matter and the associated carbon pump, whether biological (gravitational pump, e.g. [BOY 19]) or physical (mixed layer pump, e.g. [DAL 16]). – From a spatial point of view, the general cyclonic circulation, with the emergence of nutriclines in the center of the Ligurian Sea, certainly amplifies biomass cycles at certain times of the year, particularly in summer, when nutrient and light conditions are simultaneously favorable to phytoplankton. The whole ecosystem, and, consequently, the export of carbon, is probably very sensitive to this “large scale” forcing, in a way similar to the functioning of permanent domes in weaker latitudes (Guinea, Costa Rica, Angola). The North Current and its frontal zone, linked to the geostrophic circulation, are also the site of an amplification of marine life and the transfer of matter by biological or physical means (subduction pump, e.g. [LEV 12]) in the mesopelagic zone. – From an interannual point of view, we now know that each year is a new story. Winter pre-conditioning, which is highly dependent on weather events, is, by nature, different from one year to the next. The oceanic response, whether it is the dynamics of the mixing layer or the stability conditions that prevail at the start of the bloom, is highly dependent on these meteorological and physical forcings.

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– With the development of appropriate sensors, the more precise location of the different nutriclines will provide a much better understanding of the issue of chemical limitation of primary production. All these elements make the Ligurian Sea a highly attractive and easily accessible place of study, with a dimension that lends itself perfectly to continuous, integrated and multidisciplinary observation, with new tools to address these different themes with the appropriate resolutions. C.5. References [BAR 19] BARBIEUX M., UITZ J., GENTILI B. et al., “Bio-optical characterization of subsurface chlorophyll maxima in the Mediterranean Sea from a Biogeochemical-Argo float database”, Biogeosciences, vol. 16, pp. 1321–1342, 2019. [BIT 18] BITTIG H.C., STEINHOFF T., CLAUSTRE H. et al., “An alternative to static climatologies: Robust estimation of open ocean CO2 variables and nutrient concentrations from T, S, and O2 data using Bayesian neural networks”, Frontiers in Marine Science, vol. 5, 2018. [BOY 19] BOYD P.W., CLAUSTRE H., LEVY M. et al., “Multi-faceted particle pumps drive carbon sequestration in the ocean”, Nature, vol. 568, pp. 327–335, 2019. [BRU 15] BRUM J.R., IGNACIO-ESPINOZA J.C., ROUX S. et al., “Patterns and ecological drivers of ocean viral communities”, Science, vol. 348, 2015. [DAL 16] DALL’OLMO G., DINGLE J., POLIMENE L. et al., “Substantial energy input to the mesopelagic ecosystem from the seasonal mixed-layer pump”, Nature Geoscience, vol. 9, pp. 820–823, 2016. [DAN 11] DANIEL T., MANLEY J., TRENAMAN N., “The Wave Glider: Enabling a new approach to persistent ocean observation and research”, Ocean Dynamics, vol. 61, pp. 1509–1520, 2011. [DIC 05] DICKEY T.D., BIDIGARE R.R., “Interdisciplinary oceanographic observations: The wave of the future”, Scientia Marina, vol. 69, pp. 23–42, 2005. [DON 17] DONOSO K., CARLOTTI F., PAGANO M. et al., “Zooplankton community response to the winter 2013 deep convection process in the NW Mediterranean Sea”, Journal of Geophysical Research: Oceans, vol. 122, pp. 2319–2338, 2017.

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[DUR 17] DURRIEU DE MADRON X., RAMONDENC S., BERLINE L. et al., “Deep sediment resuspension and thick nepheloid layer generation by open-ocean convection”, Journal of Geophysical Research: Oceans, vol. 122, pp. 2291– 2318, 2017. [ELH 19] EL HOURANY R., SAAB M.A.A., FAOUR G. et al., “Estimation of secondary phytoplankton pigments from satellite observations using Self-Organizing Maps (SOMs)”, Journal of Geophysical Research: Oceans, vol. 124, pp. 1357–1378, 2019. [GIL 14] GILBERT J.A., JANSSON J.K., KNIGHT R., “The Earth Microbiome project: Successes and aspirations”, BMC Biology, vol. 12, 2014. [GUI 16] GUIDI L., CHAFFRON S., BITTNER L. et al., “Plankton networks driving carbon export in the oligotrophic ocean”, Nature, vol. 532, pp. 465–470, 2016. [IBA 73] IBANEZ F., “Spatio-temporal analysis of sampling process in planktology, its influence on interpretation of data by principal component analysis”, Annales de l’Institut Océanographique, vol. 49, pp. 83–111, 1973. [IBA 80] IBANEZ F., “An attempt at optimal oceanographic planification by means of linear programming”, Annales de l’Institut Oceanographique, vol. 56, pp. 97–108, 1980. [JOH 17] JOHNSON K.S., “Developing chemical sensors to observe the health of the global ocean”, 19th International Conference on Solid-State Sensors, Actuators and Microsystems (TRANSDUCERS), Kaohsiung, Taiwan, June 18–22, 2017. [KAR 11] KARSENTI E., ACINAS S.G., BORK P. et al., “A holistic approach to marine eco-systems biology”, PLoS Biology, vol. 9, p. e1001177, 2011. [LAR 14] LARSEN P.E., SCOTT N., POST A.F. et al., “Satellite remote sensing data can be used to model marine microbial metabolite turnover”, The ISME Journal, vol. 9, pp. 166–179, 2014. [LEV 12] LEVY M., FERRARI R., FRANKS P.J.S. et al., “Bringing physics to life at the submesoscale”, Geophysical Research Letters, vol. 39, 2012. [LIM 15] LIMA-MENDEZ G., FAUST K., HENRY N. et al., “Determinants of community structure in the global plankton interactome”, Science, vol. 348, 2015. [LUO 18] LUO J.Y., IRISSON J.O., GRAHAM B. et al., “Automated plankton image analysis using convolutional neural networks”, Limnology and Oceanography – Methods, vol. 16, pp. 814–827, 2018. [MAY 16] MAYOT N., D’ORTENZIO F., RIBERA D’ALCALA M. et al., “Interannual variability of the Mediterranean trophic regimes from ocean color satellites”, Biogeosciences, vol. 13, pp. 1901–1917, 2016.

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[MIG 14] MIGNOT A., CLAUSTRE H., UITZ J. et al., “Understanding the seasonal dynamics of phytoplankton biomass and the deep chlorophyll maximum in oligotrophic environments: A Bio-Argo float investigation”, Global Biogeochemical Cycles, vol. 28, pp. 856–876, 2014. [MOR 17] MORDY C.W., COKELET E.D., DE ROBERTIS A. et al., “Advances in ecosystem research: Saildrone surveys of oceanography, fish, and marine mammals in the Bering Sea”, Oceanography, vol. 30, pp. 113–115, 2017. [NIE 08] NIEWIADOMSKA K., CLAUSTRE H., PRIEUR L. et al., “Submesoscale physical-biogeochemical coupling across the Ligurian Current (Northwestern Mediterranean) using a bio-optical glider”, Limnology and Oceanography, vol. 53, pp. 2210–2225, 2008. [OLS 16] OLSEN A., KEY R.M., VAN HEUVEN S. et al., “The Global Ocean Data Analysis Project version 2 (GLODAPv2) – An internally consistent data product for the world ocean”, Earth System Science Data, vol. 8, pp. 297–323, 2016. [ORG 16] ORGANELLI E., CLAUSTRE H., BRICAUD A. et al., “A novel near-real-time quality-control procedure for radiometric profiles measured by bio-argo floats: Protocols and performances”, Journal of Atmospheric and Oceanic Technology, vol. 33, pp. 937–951, 2016. [OTT 16] OTTESEN E.A., “Probing the living ocean with ecogenomic sensors”, Current Opinion in Microbiology, vol. 31, pp. 132–139, 2016. [PIC 10] PICHERAL M., GUIDI L., STEMMANN L. et al., “The Underwater Vision Profiler 5: An advanced instrument for high spatial resolution studies of particle size spectra and zooplankton”, Limnology and Oceanography – Methods, vol. 8, pp. 462–473, 2010. [PRI 93] PRIEUR L., COPIN-MONTÉGUT C., CLAUSTRE H., “Biophysical aspects of Almofront-1. An intensive study of a geostrophic frontal jet”, Annales de l’Institut Océanographique, vol. 69, pp. 71–86, 1993. [QIN 10] QIN J.J., LI R.Q., RAES J. et al., “A human gut microbial gene catalogue established by metagenomic sequencing”, Nature, vol. 464, pp. 59–65, 2010. [RAM 16] RAMONDENC S., MADELEINEGOUTX, LOMBARD F. et al., “An initial carbon export assessment in the Mediterranean Sea based on drifting sediment traps and the Underwater Vision Profiler data sets”, Deep-Sea Research Part I – Oceanographic Research Papers, vol. 117, pp. 107–119, 2016. [REI 19] REICHSTEIN M., CAMPS-VALLS G., STEVENS B. et al., “Deep learning and process understanding for data-driven Earth system science”, Nature, vol. 566, pp. 195–204, 2019.

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[SAU 16] SAUZÈDE R., CLAUSTRE H., UITZ J. et al., “A neural network-based method for merging ocean color and Argo data to extend surface bio-optical properties to depth: Retrieval of the particulate backscattering coefficient”, Journal of Geophysical Research: Oceans, vol. 121, pp. 2552–2571, 2016. [SAU 17] SAUZÈDE R., BITTIG H.C., CLAUSTRE H. et al., “Estimates of watercolumn nutrient concentrations and carbonate system parameters in the Global Ocean: A novel approach based on neural networks”, Frontiers in Marine Science, vol. 4, 2017. [YAN 15] YANG J., RISER S.C., NYSTUEN J.A. et al., “Regional rainfall measurements using the passive aquatic listener during the SPURS field campaign”, Oceanography, vol. 28, pp. 124–133, 2015.

Acronyms

AIRWIN: Air Water Interface. A research project within the European FP5 program and launched in 2001. The aim of the project was to investigate the structure of biological communities living and growing in the sea-surface microlayer, and their role in the transport and cycling of natural organic matter. BATS: Bermuda Atlantic Time-series Study (http://bats.bios.edu). BCA: Black Carbon Aerosol (soot). BOUSSOLE: BOUée pour l’acquiSition d’une Série Optique à Long termE (http://www.obs-vlfr.fr/Boussole/html/home/home.php). CARD-FISH: CAtalyzed Reported Deposition Fluorescence In Situ Hybridization, a single-cell based method to detect specific bacterial groups. CARIOCA: NKE sensor to measure the partial pressure of dissolved CO2 in seawater in order to quantify air/ocean exchanges. CNEXO: Centre National pour l’Exploitation des Océans. CNR: Consiglio Nazionale delle Ricerche. CNRS: Centre National de la Recherche Scientifique.

The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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CO2SYS: carbonate system calculator using discrete measurements of any two of the other carbonate system parameters (total alkalinity, pH or dissolved inorganic carbon). DEWEX: DEep Water formation EXperiment was a project carried out over a full annual cycle from June 2012 to September 2013 to better characterize and understand dense water formation phenomena in the northwestern Mediterranean. DGGE: Denaturing Gradient Gel Electrophoresis usually of PCR-amplified 16S rDNA fragments separated in polyacrylamide gels with linear chemical gradients ranging from 25 to 55% denaturants that are then compared; a genetic fingerprint to profile unknown bacterial communities. DYFAMED: DYnamique des Flux Atmosphériques en MEDiterranée (https://www.seanoe.org/data/00326/43749/). ECOMARGE: ECOsystèmes des MARGEs continentales. ECOMARGE was a French research project initiated in 1983–1984. One of its main goals was the qualitative and quantitative study of particle flux and energy transfer across continental margins. EROS-2000: European River Ocean System-2000. An interdisciplinary long-term research project on biogeochemical processes in the European coastal environment, which was launched in 1988 in the framework of the European Communities’ Environmental R&D Programme. ESTOC: European Station for Time-series in the Ocean Canary islands (http://siboy.plocan.eu/ESTOC). EURATOM (or EAEC): European Atomic Energy Community. GLODAPv2: GLobal Ocean Data Analysis Project version 2 dataset. GO-SHIP: Global Ocean Ship-based Hydrographic Investigations Program (http://www.go-ship.org).

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HOT: Hawaii Ocean Time-Series (http://hahana.soest.hawaii.edu/hot/). IAEA: International Atomic Energy Agency. JGOFS: Joint Global Ocean Flux Study. LOCEAN: Laboratoire d’Océanographie et du Climat: Expérimentations et Approches Numériques. MedFlux: a collaborative research project between scientists from the U.S. and Europe, which was started in 2002 and was mainly funded by the U.S. National Science Foundation. The fieldwork took place in the Ligurian Sea at the DYFAMED long-term site. The goal of the project was to develop a seamless description of carbon fluxes and associated mineral ballast fluxes throughout the water column. MOOSE-GE: Mediterranean Ocean Observing System for the Environment – Grande Échelle. Annual cruise carried out every summer since 2010 in the north-western Mediterranean basin and supported by the MOOSE program. The objectives of the cruise are to maintain deep moorings and to monitor the physical, chemical and biological properties of water masses from surface to bottom. PFGE: Pulsed Field Gel Electrophoresis, a method to size-specifically separate DNA fragments (e.g. viruses with different genome size). PGE: Prokaryotic Growth Efficiency. RAPD: Randomly Amplified Polymorphic DNA, i.e. random amplification of genomic DNA. RAPD-PCR: RAPD Polymerase Chain Amplification (DNA amplification). SOCAT: Surface Ocean CO₂ ATlas (https://www.socat.info). SOMLIT: Service d’Observation en Milieu LITtoral (http://somlit.epoc.ubordeaux1.fr/).

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SSCP: Single Strand Conformational Polymorphism, usually of PCR-amplified 16S rDNA fragment separated in polyacrylamide gels; a genetic fingerprint to profile unknown bacterial communities. TRFLP: Terminal Restriction Fragment, Length Polymorphism, of PCR-amplified 16S rDNA fragments on polyacrylamide gels or sequencers; a genetic fingerprint to profile unknown bacterial communities. W1M3A: Fixed-Point Open Ocean Observatory in the Ligurian Sea (http://www.w1m3a.cnr.it/). WMO: World Meteorological Office (https://public.wmo.int/). WOCE: World Ocean Circulation Experiment (https://www.nodc.noaa.gov/). WoRMS: World Register of Marine Species (http://www.marinespecies.org/).

Glossary

Absorbance: a measure of the attenuation of light when passing through a material. Accessory pigments: pigments found in photosynthetic organisms that have a different molecular structure from chlorophyll-a, and absorb light of wavelengths not absorbed by chlorophyll-a. Accretion: areas on mid-oceanic ridges on which new basaltic layers are progressively emplaced during ocean opening. Adsorption: this should not be confused with absorption. It is a surface phenomenon by which atoms, ions or molecules from a liquid or gaseous phase are fixed onto a solid surface. It involves several types of processes such as low-energy van der Waals bonding, covalent or ionic chemical bonding. Desorption is the reverse of adsorption. Alkaline phosphatase: an enzyme whose catalytic function is optimal at alkaline pH. In the field of oceanography, it hydrolyzes organic forms of phosphorus to phosphate, thus allowing their assimilation by autotrophic organisms. Alkalinization: the process of making alkaline. Alkylated compounds: alkylation refers to the transfer of an alkyl group (i.e. an alkane missing one hydrogen) from one molecule to another. Alkylated compounds result from this transfer.

The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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Amorphous structure: this refers to any non-crystalline solid structure. Atoms and molecules are not organized into a well-structured lattice pattern, which makes such structures soluble, basically, and of which solubility is not dependent on pH. Ancillary variables: all core variables used in oceanography to describe the marine environment and useful here for CO2 study (e.g. T, S, O2, nutrients, Chl-a). Anomaly: a value that is different from its general long trend (annual or decadal). Apatite: a group of phosphate minerals that includes hydroxylapatite, fluorapatite and chlorapatite. Its generic formula is Ca5(PO4)3(F, Cl, OH). In general, apatite is very insoluble. Archaea: one of the three domains of life (beside Bacteria and Eukarya). Aromaticity degree: the measure of stability of a molecule, this is linked to the number of aromatic rings. Atmospheric aerosol: an aerosol is a suspension of fine solid or liquid particles in a gaseous environment (e.g. mist, airborne dust, haze). Several types of aerosols (mineral, biogenic, anthropogenic) occur in the atmosphere. They play a key role in Earth’s climate. Atmospheric deposition: this term gathers the dry deposition (gravitational deposition of airborne particles and gases) and the wet deposition (rainfall). Autotrophy: a mode of nutrition that characterizes the organisms that produce their own food using light, water, carbon dioxide or other chemical components. Autotrophs serve as primary producers in food webs, for example, plants. Auxotrophic: auxotroph organisms are unable to synthesize specific organic compounds required for their growth and rely on other organisms that produce and secrete such compounds.

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Baroclinic instability: this 3D instability occurs when a surfaceintensified geostrophic flow is meandering. It tends to restore a new geostrophic equilibrium by transporting surface water, under the current and in the trough of the meander, while the crest of the meander sees water coming from the depth to surface. Bioactive metals: in oceanography, these are metals that are needed by organisms’ growth (e.g. Fe, Cu, Co, Zn and many others). Bioavailability: availability of something (chemicals, nutrients) for living organisms. Solubility is often viewed as a proxy of bioavailability. Biogenic particles: particles produced by biological activity. Biogeochemistry: a study of the cycle in which chemical elements and substances are transferred between earth scale living systems and the environment. Biomagnification or bioamplification: this refers to the increasing concentration of any substance (here, contaminants) in the organs and tissues of an organism at higher and higher levels along a food chain. Bioregions: this refers to marine areas of which boundaries are defined by geographical and ecological characteristics. Bioturbation: this refers to the mixing, or any perturbation, of soils or sediments by living organisms (e.g. the burrowing of soils by earthworms). Blastozoid: an individual produced by asexual reproduction (budding). Bloom: fast and significant increase of algal populations. Brines: highly salty and dense sea waters. Buoyancy content: see definition in Chapter 3, Box 3.2 “The geostrophic approximation”. Carbonate system: this regroups chemical variables (total alkalinity, dissolved inorganic carbon, pH, pCO2) that control the seawater pH, the regulation of the CO2 content of the atmosphere via the biological pump,

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determine the ocean’s influence on fossil fuel CO2 uptake, and determine the extent of burial of CaCO3 in marine sediments. Chelating agents: dissolved organic compounds capable of binding a central metal ion or atom to form a coordination complex. Chromophoric dissolved organic matter (CDOM): the fraction of DOM that absorbs light at UV and visible wavelengths. Ciliates: a diverse monophyletic group of protists (unicellular eukaryotes) characterized by having cilia or ciliary structures used for swimming and feeding. Ciliates are distinguished cytologically by having two types of nuclei. Clastites (or clastic deposits): surface formations resulting from the weathering of rocks and minerals by a set of mechanical, physico-chemical or biological processes. Clastic sediments and deposits are composed of fragments of older weathered or eroded minerals and rocks. Cnidocyte: a stinging cell produced by the species of the phylum Cnidaria (Corals, medusae; siphonophores, sea anemones, hydroids) (formerly designed as nematocyte). The cnidocyte can send a kind of arrow attached to the cell with a line, which stings and maintains a prey. Coccolith-rich oozes and marls: marine sediments made from calcareous skeletons of marine micro-organisms. Colloblasts: sticking elements produced by ctenophore tentacles to secure their prey. Continental margin: progressive crustal and morphological transition between continental and oceanic domains. Convection (winter): natural convection occurs in winter when the atmospheric forcing cools sea surface, capping a layer of warm and salty layers. Coprophagy: nutritional behavior describing organisms that cover at least part of their nutritional needs by feeding on their own excrements or those of other organisms.

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Cyanophages: phages infecting cyanobacteria (former blue algae). Cyclogenesis: the formation of atmospheric cyclonic depression. Cyclonic circulation: the circulation is cyclonic when the stream horizontally curves anticlockwise in the North hemisphere. More precisely, the curl of velocity is oriented as the rotation axis of Earth when projected on the local vertical. Decay (nuclear physics): the spontaneous conversion of a nuclide into another nuclide or into another energy state of the same nuclide by emitting radiation. For a collection of atoms, the number of decay events expected to occur within a given interval of time is proportional to the number of atoms present. This decay rate is characteristic for each radionuclide. Deep convection: the main process of deep-water formation in the world’s oceans. It occurs in specific regions of high heat loss to the atmosphere. Demethylation: methylation is the bonding of a methyl group (CH3-) to a substrate. Demethylation is the reverse reaction (removal of the methyl group). Density field: three-dimensional pattern of density. Density increases with depth in the ocean except if local gravitational instability occurs temporarily. Diagnostic pigment: a noticeable pigment whose detection in water samples indicates the presence of a phytoplankton community. Diazotrophs: micro-organisms capable of assimilating molecular nitrogen (N2) by enzymatic means. For these organisms, the reservoir of nitrogen is quasi-inexhaustible. Dinoflagellates: a diverse monophyletic group of protists (unicellular eukaryotes) distinguished by the possession of two flagella typically arranged, one latitudinally and the other longitudinally, in grooves on the cell surface. Dinoflagellates are distinguished cytologically by a nucleus with condensed chromosomes. Dinoflagellates typically swim rotating about their longitudinal axis, thus spinning like a dynamo.

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Dissolved organic carbon (DOC): by convention, a complex mixture of organic molecules that passes through a 0.2 µm filter. Divalent Hg: the valence of a chemical element is the maximal number of covalent or ionic bonds it can form depending on its electronic configuration. Divalent mercury is HgII (oxidation state = 2). e ratio: the ratio between export production and total primary production as defined by Downs in his PhD dissertation (Downs, 1989). Ecological niche: a volume in a virtual multifactorial space where growth, reproduction and survival of a species is optimal. Temperature–salinity is a simple two-factor virtual space familiar to oceanographers (T–S graph). It is easy to find the niche for summer species (high T and low S) and spring species (low T and high S). Ecosystem services: benefits that humans derive from healthy ecosystems (e.g. fish stocks, O2 production, biodiversity, pollination), some of them being potentially affected by global warming and acidification. Ectoenzymatic activity: this reports on the activity of ectoenzymes (enzymes found at the surface of a cell or outside of it). The ratio between two ectoenzymatic activities characteristic of two different nutrients can be an indicator of inorganic nutrient imbalance. Ectothermic species: fishes, amphibians, reptiles and invertebrates whose regulation of body temperature depends on external sources, such as sunlight or a heated rock surface. Electronic Transport System: this refers to the transfer of electrons from electron donors to electron acceptors via redox reactions. Here, it is an indirect measurement of respiration. Endemism: the ecological state of a species being unique (not found elsewhere) to a defined geographic location or habitat type. Epipelagic: this refers to the marine surface layer in which light penetrates deep enough to allow photosynthesis. Generally, the epipelagic layer ranges from the surface to 200 m depth.

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231

Equivalent spherical diameter: a measure classically used to evaluate the size of an irregularly shaped object. It represents the diameter of a sphere of equivalent volume. Eukaryotes: organisms whose cells have a clearly defined nucleus. Euphotic zone or photic layer: in a marine ecosystem, the euphotic zone is the layer closer to the surface that receives enough light for photosynthesis to occur. Its lower depth limit is generally defined by the 1% light level. Eurythermic species: species that can tolerate a wide range of ambient temperatures. Eutrophy: the trophic state resulting from excessive enrichment of surface waters with mineral nutrients. It is characterized by the overproduction of autotrophic organisms (algae and cyanobacteria in particular). Evaporites: water-soluble minerals resulting from concentration and evaporation of aqueous solutions. Gypsum, carbonates or sand roses are evaporites. Excreta: waste matter discharged from the body, especially feces and urine. Exoskeleton: rigid or articulate envelope that supports and protects the soft tissues of certain animals, for example the hard chitinous cuticle of arthropods. Exudates: dissolved organic molecules released by phytoplankton. Exudation: the oozing of an organic liquid. In oceanography, it refers to the oozing of organic matter from phytoplankton. f ratio: the ratio of New Production to Total Production, i.e. production based on new nutrient upwelled in the euphotic zone to total production, sum of new and regenerated production. The last one is based on regenerated nutrients by biological activity (recycled by bacterial, excreted by animals). Fallout (nuclear physics): deposition of radioactive material on the Earth from the atmosphere.

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Femtoplankton: plankton organisms < 0.2 µm, in maximum dimension, exclusively viruses. Fickian-like diffusion law: Fick’s laws are used to determine the diffusion of matter. A Fick-like law can be used to obtain the diffusion coefficient. Flocculation: it is the process by which colloids form flocs or flakes. Flocs or flocculent matter: undefined aggregations of organic and inorganic matter that has a loosely clumped texture, a flocculant mass of fine particles and colloidal material. Front: separation between two water masses different in density, salinity or temperature. At the front, the horizontal gradient of density is strong. Fugacity (CO2 gas): for real gas, fugacity is defined as the pressure of an ideal gas that would have the same temperature and pressure to have the same free energy. Gabbros and chiefly basalts: volcanic rocks originating from the upper mantle and emplaced at the mid-oceanic ridge axis. Gelatinous organisms: a collective term for invertebrates characterized by a body of soft gelatinous matter, generally largely transparent; a polyphyletic group including medusae, appendicularians, siphonophores, etc. General circulation: in the ocean or in any basin, the general circulation corresponds to the pattern of the main flow. Generation time: the time between two generations, for example, the time between cell divisions in prokaryotes and protists, or time between egg hatching and egg production in copepods. Geostrophic balance: see definition in Chapter 3, Box 3.2 “The geostrophic approximation”. Geostrophic current/transport/jet: see definition in Chapter 3, Box 3.2 “The geostrophic approximation”. Gonozoid: an individual having gonads, male or female.

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Graben structures: tectonic features derived from extensive constraints leading to either crustal or sedimentary foundering. Gullies: small submarine valleys through which sediments are transiting. Heterotrophy: mode of nutrition in which organisms get their energy by consuming other organisms (plants or animals), for example ingesting prey items. Heterotrophs are secondary and tertiary consumers in food webs. HNLC marine provinces: oligotrophic regions (LC = low chlorophyll) where macronutrients (N, P, Si) are available (HN = high nutrient). Biological productivity in these areas is limited by the scarcity of micronutrients (trace metals), due to the remoteness of land-based emission sources of trace metals. Holoplankton: organisms whose entire lifecycles are completed in the plankton. Humic-like substances: organic compounds that are important components of humus. They can also be produced by biological activity (phytoplankton and bacteria) in seawater. Hydrolysis: a chemical and enzymatic reaction where a covalent bond is broken by a molecule of water. It results in the fragmentation of, for example, a polymer, and thus frees repeat units. It can occur either spontaneously or under the effect of solar radiation (UV). Hydrophilic compounds: compounds with an affinity for water, and a tendency to dissolve in it. Such compounds are ionic. Hydroxyapatite: see Apatite. Hydrozoan: species of the cnidarian group living on the bottom or in the water. Hyperpycnal flows: interstratified and dense, sediment-rich water layers. Instabilities: the ocean is almost in equilibrium. Instability occurs when one or several forces act to locally alter the equilibrium.

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Internal radius of deformation: horizontal distance from which the effect of the Coriolis force prevails over that of the pressure gradient. Then the flow direction is perpendicular to, and not in the direction of, this gradient. Isopycnal/interfacial isopycnal: a line or surface of the same density/the frontier between two water masses may be an isopycnal. Jet: intense stream, relatively narrow and thick in the same direction. Labile: in chemistry, this reports on the kinetic instability of a bond or a chemical compound. Lateralization: left–right structural or functional differences between the left and right sides of the body or the brain. Lithogenic: this reports on any material of mineral or sedimentary origin. LNLC marine provinces: the opposite of HNLC ones (LN = low nutrient). They are characterized by low concentrations of macronutrients. Macroplankton: plankton organisms ranging from 2 to 20 cm. Marine snow: relatively large aggregates of organic matter, mineral particles, dead organisms, fecal pellets, all bounded by colloids that sediment slowly. They appear from a submarine at depth like snowflakes in a winter sky. Meroplankton: organisms that are in the plankton for only part of their lifecycle (typically a larval stage), and the rest commonly spent as a benthic organism or as a member of the nekton (the swimmers). Mesopelagic: this relates to the pelagic zone between the euphotic and the aphotic (without light) zone, which is approximately between 200 m and 1000 m depth, also known as the twilight zone. Mesoplankton: plankton organisms ranging from 200 to 20,000 μm in maximum dimension. Mesotrophic: intermediate level of biological productivity between oligotrophy (i.e. low productivity) and eutrophy (i.e. excessive productivity).

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235

Metal speciation: the determination of the chemical forms or species of a metal. This mainly refers to the oxidation state, and also physico-chemistry (dissolved or particulate, complexed by organic matter or not, etc.). Metazoans: multicellular organisms. Methylation: see Demethylation. Micro-feeders: equivalent to microphagous. Microphagous: a term referring to feeding on small prey (less than 200 µm). Microplankton: plankton organisms ranging from 20 to 200 µm in maximum dimension. Mixed layer: a layer where there is no change in density, temperature and salinity. A mixed layer can be without vertical velocity. Mixing layer: the surface layer of the ocean where turbulent mixing is currently active. Mixotrophy: a trophic mode that combines both autotrophy and heterotrophy, for example photosynthesis and ingestion of prey items. Molt: a loss of feathers, hair or skin, especially as a regular feature of an animal’s lifecycle. In crustaceans, molting is the shedding of the exoskeleton, typically to let the organism grow. Morphotypes: organisms sharing a particular, distinguishable morphology, which may or may not correspond with a species, strain or race. Nanoplankton: plankton organisms ranging from 2 to 20 µm in maximum dimension. Nekton: aquatic animals that are able to swim and move independently of the currents. Neritic: a region of the oceans that extends from the low tide mark to the edge of the continental shelf.

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Niche theory: based on the hypothesis that each species in a community has a specific domain of preference in a multivariable space (an ecological niche). nr database: an online database of DNA sequences and their phylogenetic affiliation. Nutricline: the depth zone where nutrient concentrations increase rapidly with depth. The transition layer between the nutrient-rich water at the surface and the nutrient-poor water below. Nychthemeral migration: the nycthemeron is a day-long period. The two parts of the day relative to light drive the migration activity of some plankton animals. This migration, which is a vertical excursion from the depth to surface at sunset and a return trip at sunrise, is dependent on light intensity. Moon light and sun eclipses might influence this migration. Oligotrich: this usually refers to planktonic ciliates without shells or a lorica (shell) with ciliature composed of bristles or trichia, arranged in an open or full circle surrounding the mouth; typically cone-shaped or spherical. Oligotrophy: a trophic state characterized by low availability of nutritive resources and low biological productivity. OMVs: outer membrane vesicles, which are produced via budding and which may contain DNA, RNA and enzymes. OMVs have diameters ranging from 40 to 200 nm and are expected to play a key role as vectors for horizontal gene transfer. Ontogenic migration: this migration is driven by the physiology of the animal. Copepods at the end of their juvenile development migrate from the surface to a deep layer, usually at the end of summer, when food resources decline (e.g. Calanus helgolandicus in the Ligurian Sea). Oocyte: a cell that develops in an ovule. The fertilized ovule becomes an egg. Oozoid: an individual that has developed from an egg (e.g. salps). Organic ligands: see chelating agents.

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Organometallic compounds: chemical compounds that contain a covalent bound between a metal and a carbon atom within an organic group. Oxygen minimum zone (OMZ): a zone where the concentration of dissolved oxygen in seawater is at its minimum. Parapods: lateral expansion of each segment of worm’s body used to crawl on the bottom or swim in the water, usually composed of long setae or paddle. Partial pressure (CO2 gas): this is defined as the product of CO2 mole fraction and total pressure and this is expressed in µatm. In practice, the correction for the non-ideal nature of CO2 gas is negligible (< 1 µatm) and CO2 partial pressure is often treated identically to its fugacity. Petrogenic hydrocarbons: hydrocarbon compounds associated with products derived from petroleum or petroleum sources. Phages: bacterial viruses. Philopatric: an organism that has the tendency to stay in, or habitually returns to, a particular area. Phorozoid: an individual asexually produced by the oozoid of a doliolid species that has the role of collecting food to maintain the colony like an old oozoid. Phospholipids: lipids (i.e. a biomolecule that is soluble in nonpolar solvents) generally consisting of hydrophobic fatty acids and a phosphate group. Photic layer: the marine surface layer whose solar illumination allows algal development. Photobleaching: photochemical degradation of fluorophores leading to a decrease (or loss) of fluorescence. Photoprotection: mechanisms to protect the photosynthetic apparatus of phytoplankton cells from damages caused by strong light intensity. Photoreduction: reduction reaction induced by light.

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Phylotype: typically, bacteria with the same or a very similar 16S rDNA sequence (often used as a proxy for bacterial species). Physiographic characteristics: morphological characteristics of a domain (aerial or submarine). Picoplankton: plankton organisms ranging from 0.2 to 2 µm in maximum dimension. Pigment: phytoplankton cells contain pigments to absorb light energy in order to perform, for example, photosynthesis. Chlorophyll-a is the primary pigment used in photosynthesis. Plankton: living organisms in the water column whose motility is insufficient to overcome currents and movements of water masses. Pneumatophore: siphonophore polyp that produces and stores gas in such a way as to give buoyancy to the colony. Specially developed in the genus Physalia. Polycondensation: a polymerization process that occurs by condensation, i.e. by steps (monomers give dimers, then trimers, etc.). Polycondensation is to be distinguished from chain-growth polymerization. Polyp: an individual with a stomach cavity that is usually connected to the other individual, in the colony. The mouth, surrounded by tentacles covered with cnidocysts and designed to catch prey, is also used to evacuate the undigested food. Polyphosphates: salts or esters formed from the structural unit orthophosphate having linear or cyclic structures. Potential temperature: the temperature of a water mass that has been adiabatically moved (i.e. without heat exchange with the environment) to a reference pressure. Prokaryotes: single-celled organisms that have no distinct nucleus with a membrane. Protists: a hyper-diverse group of unicellular eukaryotes.

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239

Pyrolytic hydrocarbons: hydrocarbons generated by the thermal decomposition of organic compounds in the absence of oxygen, to avoid oxidation and combustion. Radiolarians: protists, mostly marine and planktonic, amoeboid with skeletons of opaline silica. Radionuclides: radioactive nuclides. Nuclides are atoms characterized by the composition of their nucleus (i.e. their number of protons and neutrons). Reactive orthophosphate (PO43-): the structural unit of phosphorus that is most easily assimilated by autotrophic organisms. Recruitment: in biology, when a juvenile organism joins a population, whether by birth or immigration, usually at a stage whereby the organisms are settled and able to be detected by an observer. In the study of fisheries, recruitment refers to the number of fishes surviving to enter the fishery or to some life history stage such as settlement or maturity. Remineralization: a conversion of organic matter into nutrients by bacteria. Residence time: this measures the average time spent by a molecule of water in a reservoir. The residence time defined for steady-state systems is equal to the reservoir volume divided by the inflow or outflow rate. Residual buoyancy: see definition in Chapter 3, Box 3.2 “The geostrophic approximation”. Resilience: in ecology, resilience is the capacity of an ecosystem to respond to a perturbation or disturbance by withstanding damage and recovering quickly. Revertant strains: bacterial strains that exhibit genetic features they obtained from other bacterial strains via horizontal gene transfer, as achieved by exposition to outer membrane vesicles. Rias: submerged former aerial valleys.

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Rifting: surface signature (series of grabens) of crustal processes leading to continental breaking. Roseophage: bacterial virus infecting the genus Roseobacter. Salt diapirs: ascending sedimentary deformations due to the presence of interstratified salt layers. Scars: typical marine morphologies due to sedimentary instabilities and failures. Sediment trap: a device for collecting sinking particles in the water column. The sinking material is caught at a recorded depth in a “funnel”-like tube of a known area and over a defined length of time. Sentinel species: species that act as indicators of a danger to human life or of an ecosystem damage by providing advance warning of danger. Septum (pl. septa): a membrane that separates two parts of a cell or an organ. Seta (pl. setae): a kind of short hair or bristle. Shear: vectorial difference of velocity between two depths or two locations (dimension: s-1). Somites: body segments of a copepod. Stoichiometry: molar proportions of chemical compounds or elements in a chemical formula or in a chemical reaction. It is based on the law of conservation of mass. Stolon: an expansion of the body built with different tissues of the animal (ectoderm, endoderm and/or mesoderm) on which buds appear, giving a new individual or are transported from a producing site. Stolon is also the plumbing or network of feeding tubes and nerves joining the different individuals in a colony of individuals. Stratification of the water column: superimposition of water layers of different densities and properties (temperature, salinity, oxygenation) that

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241

prevents water mixing and homogenization. It mostly results from the action of heat and evaporation. Subduction: progressive disappearance of an oceanic crust below either a continent or another domain of oceanic crust. Subsidence: slow foundering of a crustal, or oceanic, domain and its sedimentary covers, as consequence of its progressive cooling. Suspensivore (mode): an organism that feeds on suspended material. Symbiont: an organism living in a state of symbiosis, i.e. with another organism. Synrift units: sedimentary units deposited during rifting processes. Taxon: taxonomic unit of any rank (species, genus, family, etc.). Terrigenous fans: deep “fan-shaped” sedimentary units deposited along continental slopes. Thermocline: physical barrier materializing a strong change of temperature with depth, generally in the upper layer. Tintinnid: a ciliate of the order Choreotrichida and suborder Tintinnidia characterized by the possession of a lorica (shell) into which the ciliate can withdraw into. Trace metals: metals found in very low concentrations (traces). Transductants: bacterial cells into which new genetic material has been transduced, usually by a bacteriophage that experienced a faulty DNA-assembly by incorporating bacterial host DNA instead of viral DNA before its release during the lytic cycle (revertant strain). Transparent exopolymeric particles (TEP): a class of organic aggregates (particles) with specific staining properties. Turn-over time: a period of time necessary to change all the quantity of the variable considered.

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Umbrella species: species useful for making conservation-related decisions, typically because protecting them indirectly protects the many other species living in the ecological community of their habitat. Upwelling: wind-driven motion of dense, cold and nutrient-rich water masses towards the ocean surface. Owing to their high concentration in plankton, upwelled waters are characterized by high fishery production. Ventilation: a process by which “young” surface waters, which have recently been in contact with the atmosphere, are injected into the ocean interior and exported away from their sources (for instance, supply of oxygen to deep water by downwelling or mixing processes). Viral lysis: lysis of cells by viruses, resulting in the death of the cell, the release of newly formed viruses, cell content and cell debris. Zooid: an individual. A general term to which (blast-, oo-, phoro-, gono-) is usually added, to indicate its origin or role.

List of Authors

Hervé CLAUSTRE LOV SU/CNRS Villefranche-sur-Mer France Daniel COSSA ISTerre Grenoble Alpes University France Janine CUZIN LOV SU/CNRS Villefranche-sur-Mer France John DOLAN LOV SU/CNRS Villefranche-sur-Mer France Aurélie DUFOUR MIO Aix-Marseille University Marseille France

Scott W. FOWLER School of Marine and Atmospheric Sciences Stony Brook University New York USA Jean-Marc FROMENTIN MARBEC IFREMER Montpellier France Beat GASSER Environment Laboratories IAEA Monaco Jacqueline GOY MNHN Paris France Lionel GUIDI LOV SU/CNRS Villefranche-sur-Mer France

The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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Lars-Éric HEIMBÜRGER-BOAVIDA MIO Aix-Marseille University Marseille France

Virginie RAYBAUD ECOSEAS Côte d’Azur University Nice France

Fabien LOMBARD LOV SU/CNRS Villefranche-sur-Mer France

Chiara SANTINELLI Istituto di Biofisica CNR Pisa Italy

Christophe MIGON LOV SU/CNRS Villefranche-sur-Mer France

Antoine SCIANDRA LOV SU/CNRS Villefranche-sur-Mer France

Juan-Carlos MIQUEL Institute Bobby Cap d’Ail France

Lars STEMMANN LOV SU/CNRS Villefranche-sur-Mer France

Paul NIVAL LOV SU/CNRS Villefranche-sur-Mer France

Maurizio WÜRTZ UNIGE Genoa Italy

Index

A, B, C aggregation/disaggregation, 38, 40, 47, 49, 50, 52, 54 artificial intelligence, 207, 211, 214–216 atmospheric deposition, 177, 178, 183, 188 autonomous vehicles, 207 bioaccumulation, 197 bioavailability, 175, 179, 183, 197 biological carbon pump, 35, 46, 56 carbon export, 9, 16, 19, 23 carbon pump, 216 CDOM (chromophoric dissolved organic matter), 3, 14, 15, 23, 24 cnidarians, 119 copepod, 70, 71, 73, 74, 89–93, 95–98 ctenophores, 124, 125, 126 D, E, F decadal trends, 193, 196 deep water convection, 213 dinoflagellates, 70–72, 75, 86, 87

export flux, 42, 44–46, 48, 53 fecal pellets, 31, 32, 34, 38, 40–42, 49–52, 54 G, H, I gliders, 207, 209–211 grazing, 71, 79 heterotrophic prokaryotes, 1, 2, 14, 15, 18, 19, 23 humic-like substances, 3, 15 imaging, 212–215 L, M, O lability, 2–4, 13, 24 marine mammals, 148, 162, 164 marine snow, 32, 37, 40, 52 mercury, 175, 178–183, 194, 196, 197 mesopelagic fish, 154–159, 165 micronekton, 126, 129, 131 mineralization, 2, 9, 17, 19 mixing layer, 216 mixotrophy, 68–72, 80, 81, 86 organic chemical contaminants, 175, 189, 192, 193, 196, 197

The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

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P, R, S particle feeders, 111 plankton meso-, 68, 70, 71 micro-, 68, 70–72 nano-, 68–71 predator, 109, 111–116, 119, 120, 122, 123, 125, 127–130 profiling floats, 207, 209, 211 radiolarian, 70, 71, 86, 88 radionuclides, 31, 34, 42, 48, 54, 55 anthropogenic, 175, 185, 187, 188, 196, 197 ray, 159 respiration rates, 16 sampling, 68, 75, 76, 82, 84, 92, 93 satellite, 207–209, 213 scavenging, 48, 49 sea turtles, 148, 161, 162, 165 seamounts, 155, 164 sediment trap, 31, 33, 34, 40, 41, 43, 46, 48, 49, 51, 52, 54, 55 settling velocity, 45, 47

sharks, 148, 149, 159, 160 sinking particles, 31, 32, 34, 40, 42, 44, 48, 49, 53–55 spatial distribution, 112 squids, 148–152 stoichiometry, 15 stratification, 216 surface circulation, 13, 22 swordfish, 150, 154–156, 160 T, V taxonomy, 73, 74, 77, 109, 116, 119, 133 Thaliacean, 116, 117, 126 time variation, 122 trace metals, 175, 177–179, 193, 195–197 tributyltin, 175, 184 tuna bluefin, 149, 152–155 small, 153, 154 turnover time, 2, 11 vertical migration, 94, 95, 98 vertical transfer, 197

Summary of Volume 1

Preface Chapter 1. The Development of Knowledge of the Ligurian Sea Paul NIVAL 1.1. The first naturalists on the shores of the Ligurian Sea 1.2. Vertical structure of the Mediterranean and hydrodynamics 1.3. Flow rate of the Ligurian Current 1.4. Mesoscale structures in the Ligurian Sea: hydrodynamic front and the search for spatial precision 1.5. The seabed and living species 1.6. Study of chemical substances in the Ligurian Sea 1.7. Towards a synoptic vision of the Ligurian Sea. Remote sensing 1.8. Towards continuous observation and environmental monitoring 1.9. References Chapter 2. The Ligurian Basin: A Geomorphologic and Geological Background Jean MASCLE, Sébastien MIGEON and Virginie HASSOUN 2.1. Introduction 2.2. Geographic and geological boundaries 2.3. Origin and geological evolution of the Ligurian basin and of its margins: a brief review 2.3.1. Birth of the Ligurian basin 2.3.2. Creation and evolution of the Ligurian Sea continental margins The Mediterranean Sea in the Era of Global Change 2: 30 Years of Multidisciplinary Study of the Ligurian Sea, First Edition. Edited by Christophe Migon, Paul Nival and Antoine Sciandra. © ISTE Ltd 2020. Published by ISTE Ltd and John Wiley & Sons, Inc.

The Mediterranean Sea in the Era of Global Change 2

2.4. Morphology of the Ligurian Sea 2.4.1. General morphology 2.4.2. Submarine canyons 2.5. Sedimentary cover and sedimentary processes 2.5.1. Evolution of the sedimentary cover 2.5.2. Prevailing sedimentary mechanisms 2.6. A few concluding remarks 2.7. References Chapter 3. Physical Oceanography of the Ligurian Sea Louis PRIEUR, Fabrizio D’ORTENZIO, Vincent TAILLANDIER and Pierre TESTOR 3.1. Introduction 3.2. Circulation patterns from large scale to frontal dynamics 3.3. Observation time series: sentinel of the Mediterranean Sea 3.4. Discussion and conclusion 3.5. References Chapter 4. The Carbonate System in the Ligurian Sea Laurent COPPOLA, Jacqueline BOUTIN, Jean-Pierre GATTUSO, Dominique LEFEVRE and Nicolas METZL 4.1. Introduction 4.2. Distribution of the carbonate system in the Ligurian Sea 4.3. The seasonal cycle in surface water 4.4. Long-term changes in the carbonate system and acidification 4.4.1. Surface trends 4.4.2. Interior trends 4.5. Changes in the carbonate system in the Ligurian Sea in the Mediterranean Sea and global contexts 4.6. Conclusion 4.7. Acknowledgments 4.8. References Chapter 5. Emission Sources, Fluxes and Spatiotemporal Distribution of Nutritive Resources Christophe MIGON, Orens PASQUERON DE FOMMERVAULT and Fayçal KESSOURI 5.1. Introduction 5.2. What is required for biological development? 5.3. Sources of nutrients 5.3.1. External sources

Summary of Volume 1

5.3.2. Inputs from deep layers 5.3.3. Budgets 5.4. Seasonal patterns 5.5. Spatial distribution 5.6. Chemical limitation of primary production 5.6.1. The Redfield model 5.6.2. Peculiarity of N:P molar ratios in the Ligurian area 5.6.3. Model of P-limitation 5.7. Decadal trends and possible consequences for regional productivity 5.8. Concluding remarks 5.9. References Chapter 6. Primary Production in the Ligurian Sea Nicolas MAYOT, Paul NIVAL and Marina LEVY 6.1. Annual cycle of phytoplankton biomass, production and community structure in the Ligurian Sea 6.1.1. Regional context of the area 6.1.2. The diversity of phytoplankton species: the base of community ecology 6.1.3. Phytoplankton community structure 6.2. From the influence of small spatiotemporal features to the interannual and long-term variability 6.3. Modeling the impact of the physics on phytoplankton growth and distribution 6.4. References Chapter 7. Pelagic Viruses, Bacteria and Archaea Markus WEINBAUER and Branko VELIMIROV 7.1. Background 7.1.1. Microbial food webs 7.1.2. Microbe-mediated ecosystem functions and biogeochemical cycles 7.2. Study sites 7.3. Diel variability of micro-organisms 7.4. Seasonal variability of micro-organisms 7.5. Variability of micro-organisms: sunlight versus dark ocean 7.6. Effect of episodic events on micro-organisms: upwelling and aerosols 7.6.1. Upwelling 7.6.2. Sahara dust aerosols

The Mediterranean Sea in the Era of Global Change 2

7.6.3. Volcano ash aerosols 7.6.4. Black carbon-rich aerosols 7.6.5. Conclusions 7.7. Effect of turbulence on micro-organisms 7.8. Effect of global warming and ocean acidification on micro-organisms 7.9. Effect of P-limitation on micro-organisms 7.10. Effect of viral lysis and flagellate grazing on prokaryotic diversity and growth 7.11. Nanobacteria, ultramicrobacteria and starvation forms 7.12. Microbial diversity hypothesis 7.13. Horizontal gene transfer 7.14. Acknowledgments 7.15. References

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