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Finding new life.

The European Census of Marine LifeDiversity of European Seas -

Finding New Life

Finding new life.

AcknowledgementsBhavani E NarayanaswamyScottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, UK

Henn OjaveerEstonian Marine Institute, University of Tartu, Parnu, Estonia Geoff BoxshallDepartment of Zoology, The Natural History Museum, Cromwell Road, London, UK

Ward AppeltansFlanders Marine Institute, Wandelaarkaai 7, Oostende, Belgium

Roberto DanovaroPolytechnic University of Marche, Via Brecce Bianche, Ancona, Italy

Poul Holm Trinity Long Room Hub, Trinity College Dublin, Ireland Thom NickellScottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, UK

The European Census of Marine Life was funded by a number of different sources. In particular we would like to acknowledge the support given to us by Foundation TOTAL, the Alfred P Sloan Foundation, the Stavros Niarchos Foundation and Argyll and Islands Enterprise. In addition much of this work would not have been able to be undertaken had it not been for the research undertaken by the numerous scientists working in European Waters, the support given by the different European marine science Institutions and Universities, as well as the funding agencies in each country.

For all correspondence relating to this report please contact [email protected]

For more information, please visit www.eurocoml.org

Images courtesy of J Stafford-Deitsch, R Hopcroft, B Bluhm, K Iken, H Brown, D Fiege, K Rascoff.

Authors

EditorsBhavani E Narayanaswamy, Olga Kimmins and Henn Ojaveer.

CitationNarayanaswamy, BE, Ojaveer H, Boxshall G, Appeltans W, Danovaro R, Holm P and Nickell T. (2010) Diversity of European Seas - Finding New Life. EuroCoML Non-Technical Report, Oban, UK.

Finding new life.

Preface 5

Introduction 8 History of Marine Animal Populations 14

Species Abundance, Diversity, Distribution 20

Zooming in on the detail 24

Biodiversity in European Seas 37

Alien species 44

Legacies 53

Contents:

References 54

Finding new life.

Preface 5





Alien species 44

Legacies 53

Contents:

References 54

Finding new life.

Preface

It gives me great pleasure to introduce the work of the European regional committee of the Census of Marine Life (EuroCoML) as part of the celebration of its “Decade of Discovery” this year. Although EuroCoML had its first meeting in 2003, the global programme started earlier in 2000 and discussions about how such a vast endeavour could be instigated started some time before with senior marine scientists. The fact that the Census programme has been such a success is down to the hard work of the nearly 3,000 researchers involved from more than 80 nations. Alongside the Census field projects, and the projects exploring the history and trying to make predictions for the future, have been the 13National and Regional Implementation Committees (NRICs), of which Europe is one. One of the NRICs main roles has been to promote the Census to researchers, the public and other stakeholders within their countries and regions. This was just one of Europe’s main aims. Europe has been extremely successful in working with the projects already running within the Census framework as well as highlighting areas of research that are of particular importance to Europe, for example the impact of invasive alien species. Through collaborative research, it has been found that there are likely to be more than 1,200 alien species in European waters alone, several hundred more than were previously thought. Other work highlighted by researchers in Europe has been the changes in fish communities in European waters over numerous centuries. Some of this information is being used to help forecast what fish species may inhabit European waters as air and sea temperatures rise. At the start of the Census ~29,000 marine species were known in European waters and as the “Decade of Discovery” peaks, we now estimate that there are almost 32,000 species living in European seas! These discoveries have also highlighted where there are gaps in our knowledge; in European waters at least, future research should begin to concentrate more on the smaller fauna. The new results gathered on biodiversity should now be used when designing marine management strategies and policies as well as when making management decisions.

European researchers have not limited their studies to the shelf seas surrounding our coun-tries. In the deep waters of the world’s oceans five deep-water Census projects and EuroCoML have worked closely together over the past five years to bring the deep sea into the public domain. The outcome of this collaboration has resulted in numerous high-profile outcomes, notably the book, “Deeper than Light” which is available in five different languages, and an exhibition, “Deep Sea Life” which opened in the Smithsonian Museum of Natural History earlier this year. A further joint venture between EuroCoML and the Biogeography of Deep-water Chemosynthetic Ecosystems resulted in an animation, “Exploring the Ocean Depths” being produced.

Finding new life.

Preface 5





Alien species 44

Legacies 53

Contents:

References 54

Finding new life.

Preface 5





Alien species 44

Legacies 53

Contents:

References 54

Public perception and appreciation of the oceans is growing, even without the events in the Gulf of Mexico this year. The incredible value brought by a programme, such as the Census of Marine Life, which eschews normal “hypothesis-driven” research favoured by funding agencies in contrast to invigorating the spirit of discovery, has truly forged a bond between European marine scientists and our colleagues around the world. I was fortunate to have the opportunity to chair the EuroCoML for over five years and to see the programme and its discoveries grow year by year. This would not have been possible without the dedication of the programme manager, Bhavani Narayanaswamy, and the whole steering committee. I would also like to pay tribute and honour the late Professor Alasdair McIntyre for his vision and guidance, and my successor Henn Ojaveer and his co-chair Isabel Sousa-Pinto, for steering us all to a successful conclusion that truly marks a Decade of Discovery.

Professor Graham Shimmield, Former Chair, European Census of Marine LifeBigelow Laboratory for Ocean Sciences

Finding new life.

Preface 5





Alien species 44

Legacies 53

Contents:

References 54

Finding new life.

Preface 5





Alien species 44

Legacies 53

Contents:

References 54

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Hermit crab walking on a seastar in UK waters. Image courtesy of H. Brown.

Mako shark. Image courtesy of J Stafford-Deitsch.

Public perception and appreciation of the oceans is growing, even without the events in the Gulf of Mexico this year. The incredible value brought by a programme, such as the Census of Marine Life, which eschews normal “hypothesis-driven” research favoured by funding agencies in contrast to invigorating the spirit of discovery, has truly forged a bond between European marine scientists and our colleagues around the world. I was fortunate to have the opportunity to chair the EuroCoML for over five years and to see the programme and its discoveries grow year by year. This would not have been possible without the dedication of the programme manager, Bhavani Narayanaswamy, and the whole steering committee. I would also like to pay tribute and honour the late Professor Alasdair McIntyre for his vision and guidance, and my successor Henn Ojaveer and his co-chair Isabel Sousa-Pinto, for steering us all to a successful conclusion that truly marks a Decade of Discovery.

Professor Graham Shimmield, Former Chair, European Census of Marine LifeBigelow Laboratory for Ocean Sciences

Finding new life.

Preface 5





Alien species 44

Legacies 53

Contents:

References 54

Finding new life.

Preface 5





Alien species 44

Legacies 53

Contents:

References 54

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Introduction WHAT IS THE CENSUS OF MARINE

LIFE?

The Census of Marine Life is a growing global network of researchers from more than 80 nations that have been involved in a ten-year (2000-2010) scientific initiative. WHY THE NEED FOR A CENSUS OF

MARINE LIFE?

About 70% of the Earth’s surface is covered by ocean and of this it is estimated that only 5% of the ocean has been explored. By comparison to the land, relatively little is known about the animals living in the world’s oceans, and even less about those that inhabit the depths of the ocean; more than half the ocean is deeper than 3,000 metres. Much of the research that has previously been undertaken has concentrated mainly on the more accessible near-shore regions and down to a depth of about 1,000 metres. To increase our knowledge and understanding of the life that inhabits the world’s oceans, the Census of Marine Life was formed. The overarching aim of the Census is to both assess and explain the diversity, distribution and abundance of life in the oceans. Within this framework the Census proposed what appears to be three very simple and straightforward questions and upon which the foundations of the Census has been built. They were:

• What did live in the oceans? • What does live in the oceans? • What will live in the oceans?

Prior to the Census of Marine Life, the lists of species held by different institutions around the world was accessible to a limited number of people. Through the Census, the Ocean Biogeographic Information System (OBIS; http://www.iobis.org) was formed and scientists and researchers with access to species lists were asked to add/send data to OBIS. Europe also has its own OBIS called EurOBIS (http://www.marbef.org/data/eurobis.php) maintained by the Flanders Marine Institute. It is through this that scientists, non-government organisations and other stakeholders have

become more aware of the lack of data in certain areas and depths of the oceans. With regards to diversity there are numerous lists and collections of specimens residing in natural history museums, laboratories and other institutions. It has been estimated that about 230,000 marine species have so far been described with more than 5,500 added by Census researchers since 2000. It is hoped that by the end of 2010 most of the old species records and all of the new ones will have been entered into the database. Not only is it hoped for all the data to be in OBIS but for every species to have an entry in the Encyclopaedia of Life (www.eol.org), whereby pictures, references and general information for every species, both marine and terrestrial, can be found. Species diversity does not always remain static with changes in diversity attributed to many different factors including changes in the world’s climate as well as fishing. Hot spots of diversity occur in the oceans just like they occur on land, particularly for the larger animals such as fish. By finding out more information about these hotspots it is hoped that these larger animals may be protected. The distribution of species has become even more important as old records have been investigated. Of particular interest is the change in species range and territory and trying to find the reasons as to why this is occurring; is it due to changes in climate? Abundance was the third aspect of importance to the Census. Researchers were not only interested in the diversity and distribution of the fauna, but also in trying to determine how many individuals of each species there were in different regions. In the marine science community, both actual numbers of a species and also its weight (biomass) are of interest. 14 field programmes were instigated by the Census of Marine Life; many of those either have a scientific project running within Europe, or have European researchers involved (see text box). The projects cover:

• The whole size spectrum of organisms, ranging from microbes to whales;

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Serpulid worm from the Mediterranean. Image courtesy of H. Brown.

Feather star from the West coast of Scotland. Image courtesy of H. Brown.

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• The vast depth range from the shore line to the deep-sea;

• The tropics to the poles; • A number of different habitats from

underwater mountains (seamounts) to the vast expanse of the abyssal plains;

• Employ a variety of technology ranging from placing tags that capture environmental and biological data on individual animals to cameras that film/take still images of animals in their home environment to genetic techniques that can be used on larvae/animal fragments to help with their identification.

WHY THE NEED FOR A EUROPEAN

CENSUS OF MARINE LIFE?

The European Census of Marine Life (EuroCoML) is a Regional Implementation Committee for the Census. National and Regional Implementation Committees (NRICs) were formed to assess the known, unknown and unknowable about marine biodiversity in local waters. In addition it was anticipated that the NRICs would be able to ensure that the aims, results and outcomes of the Census reached as wide an audience as possible, including scientists, non-government organisations and the general public amongst others. EuroCoML is one of 13 NRI committees that were formed with the remit to support, promote and synthesise results that address the environmental and societal needs of communities within their region of operation. As can be seen from the map (p.14), EuroCoML covers one of the largest areas of all the NRICs; from Greenland in the west to Vladivostok in the east and from the Mediterranean Sea in the south to the Arctic in the north (includes the Arctic, North Sea, Baltic Sea and North East Atlantic to the Mid Atlantic Ridge). Most countries within Europe have at least one scientist engaged with projects connected to the Census of Marine Life. Fig. 2 also highlights many of the research institutes undertaking marine science within Europe. Within the Census framework, EuroCoML has its own specific aims. These are to:

• Expand partnerships and coordination with relevant European programmes and organisations also in tandem with the general growth of the CoML;

• Increase European participation in several particular CoML projects where untapped potential remains;

• Improve marine taxonomy and species data in the European region;

• Improve biodiversity and ecosystem information for applied resource management in waters where European nations hold major influence;

• Improve awareness of the Census with the wider public.

EuroCoML was successful in the aims listed above, particularly in making links with programmes already funded and running in Europe. These included the EU Network of Excellence – Marine Biodiversity and Ecosystem Functioning (www.marbef.org), the EU FP6 programme Hotspot Research on the Margins of European Seas (www.eu-hermes.net) and its daughter programme Hotspot Ecosystem Research and Man’s Impact on European Seas (www.eu-hermione.net), to name but a few. EuroCoML was also very active in promoting the results from the Census and engaging with the public by giving talks, producing posters, flyers and newsletters to a wide range of audience types (www.eurocoml.org). As the first Census draws to a close at the end of 2010 it is hoped that the data that have been gathered and the results that have been synthesised will:

• Advance the knowledge of life in the world’s ocean;

• Produce a catalogue of marine species;

• Help provide information so that decisions relating to managing marine resources can be carefully undertaken.

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A mass of brightly coloured soft coral, interspersed with cup coral and brittle stars along the Wyville-Thomson Ridge, UK waters. Image courtesy of Department for Business, Innovation and Skills (formerly DTI).

Serpulid worm found in Mediterranean waters. Image courtesy of H. Brown.

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CENSUS OF MARINE LIFE PROGRAMMES: Abyssal Plains: documenting abyssal plains species diversity; Antarctic Ocean: surveying biodiversity of the cold Antarctic waters; Arctic Ocean: a biodiversity inventory of the fauna in Arctic sea ice, water column and sea floor; Continental Margins: explaining biodiversity pattern on gradient dominated margins; Continental Shelves: study Pacific Salmon migration routes using tagging technology; Coral Reefs: enhance global understanding of reef biodiversity; Microbes: index and organise what is currently known about microbes; Mid-Ocean Ridges: exploratory study of animals inhabiting the northern mid-Atlantic; Near Shore: inventory and monitor biodiversity at depths of less than 20 metres; Regional Ecosystems: biodiversity patterns and processes in the Gulf of Maine; Seamounts: global investigation of seamount ecosystems; Top Predators: study migration patterns of open ocean animals using tagging technology; Vents and Seeps: global study of biogeography of deep water chemosynthetic ecosystems; Zooplankton: a biodiversity assessment of animal plankton; Oceans Past: analysing marine populations using historical archives pre- and post significant human impacts on the ocean; Oceans Future: describe and synthesise globally changing patterns of species abundance, distribution, and diversity; Information systems: a global geo-referenced database of marine species; EuroCoML AFFILIATED PROJECTS: Coastal Biodiversity: Environmental Modulation of Biodiversity and Ecosystem Dynamics; Invasive Species: Determining level of invasive alien species in European waters; Tracking Atlantic Predators: describe and understand behaviour and movements of large vertebrates.

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Fig. 1. NRIC Regions and Sub-Regions. Image courtesy of M. Costello Fig. 2. Marine Research Institutes in Europe. Image courtesy of M. Coll

NE Atlantic Ocean

Arctic Sea

North Sea

Baltic Sea

Mediterranean

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History of Marine Animal Populations

HOW MAY WE LEARN FROM HISTORY?

To understand the interaction of humans and the oceans we need to bridge the divide between history and science. Historical research can provide baselines of ocean abundance and species distribution in the past and inform us of the scale of human impact through time. Historical research will inform us of how much society depended on ocean resources for economic, social and cultural needs. We need this knowledge not only to understand our past but also to predict ocean resilience in the future. The History of Marine Animal Populations (HMAP) project was constituted as four sub-groups for the seas around Europe: the North Sea, the Baltic, the Mediterranean and the Black Sea, and the White and Barents Seas. Thanks to the collaborative efforts we are now in a position to begin to piece together a picture of human interaction with marine life in the European seas in the past 500-2,000 years. We now know enough to quantify the removals by human exploitation of several commercial target species. We have a good sense of the importance of human interaction for the nearshore ecosystems, are beginning to understand the importance of marine products for human consumption, and have a much better basis from which to assess the main drivers of human marine exploitation. These insights are critical not only to our understanding of the past but also to management in the 21st century, when the oceans will be the last part of the biosphere to be exposed to a change from hunting to cultivating practices. The breakthrough is due to the introduction of established marine science methodology to historical data, notably standardising fishing effort (catch-per-unit effort), zoo-archaeological analysis of marine animal remains, biodiversity counts of historical fisheries, statistical modelling of historical data, etc.

INSIGHTS FROM MONASTIC RECORDS – THE WHITE AND

BARENTS SEA

On the shores of the White and Barents seas in northern Russia, Orthodox monks have kept meticulous records of the landings from the sea and rivers in the area since the 16th century. Atlantic salmon was one of the most valuable products of the local economy, being extracted mostly in the lower parts of rivers, using weirs that remained technologically unchanged over the centuries. This makes fishing effort measurable over time and allows comparison of historical catch data for the 17th and 18th centuries with the statistical data that are available from the end of the 19th century. The study based on historical catch data from several locations showed that size of salmon populations in the Russian North before the mid-20th century depended mostly on climatic fluctuations, with salmon abundance increasing in warmer periods. After about 1950, most populations declined due to overfishing, the development of timber industry, dams and pollution. Signs of climate-related dynamics were observed also on other fish, such as cod, halibut and herring, although correlation did not approach statistical significance. In particular, the White Sea herring fishery, of economic importance since the 18th century, showed considerable short-term fluctuations of catches due to both social and natural factors and their interaction, which may confound climate effects. Climate effects were also pronounced on Arctic marine mammals such as white whales, Greenlandic seals, narwhales and others, which considerably changed their distribution patterns migrating to more southern regions than usual in cold periods of 1800-1809 and 1877-1903, and again in 1970-80. For marine mammals anthropogenic pressure became a significant factor earlier than for fish. Hunting impacted the general dynamics of the population of the eastern walrus from at least the 17th century and may explain changes in its distribution range over several centuries. However, the walrus population was able to sustain itself as long as remote islands such as Franz Josef Land were not yet discovered by humans. Improvements of navigation and

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hunting techniques in the late 19th century resulted in a considerable decrease of the walrus population by the middle of the 20th century. For fish, particularly for Atlantic salmon, clear stress signals related to human activities such as overfishing and development of forestry with timber-rafting became apparent only by the end of the 19th century.

INSIGHTS FROM FISH BONES Some climate models predict that air and sea temperatures will rise by approximately 3°C during the next 70-100 years. In order to understand some of the processes by which suggested global warming might affect marine fish species near Denmark, researchers have investigated the fish fauna during one of the warmest prehistoric periods, the warm Atlantic period (around 7000-3900 BC). A total of 108,000 fish bones were identified, and amongst them were bones of many species, for example anchovy and black sea bream, which we usually consider to be typical of waters much farther south and warmer, like the Mediterranean Sea. When temperatures cooled after the warm period ended, most of these species disappeared from the archaeological record, suggesting that local abundances declined. However, many of those same warm-water species have recently reappeared in waters around Denmark as temperatures have risen in the last 10-15 years. The archaeological information can be an indicator of which species may become common as climate changes and warms. The period circa 950-1050 saw a major rise in fish consumption around the North Sea. Early medieval sites are dominated by freshwater and migratory species such as eel and salmon, while later settlements reveal a widespread consumption of marine species such as herring, cod, hake, saithe and ling. The “fish event” of the 11th century reflected major economic and technological changes in coastal settlements and technologies and formed the basis of dietary preferences that were to last into the 17th century. The evidence also supports a hypothesis that sea-going vessels were in wide use by the 13th century, catching deep-sea fishes such as ling which would require lines of several hundred metres. Commercial fisheries were well established by the High Middle Ages and would feed a European population which by the same time had developed religious practices of fasting and abstinence of red meat in favour of fish at

certain weekdays and through the forty weekdays of Lent. AN ANCIENT FISHING INDUSTRY – THE MEDITERRANEAN AND BLACK

SEAS The Mediterranean and Black Sea are among the earliest heavily fished marine ecosystems in the world. Fish was an important source of food in the coastal and riverine cultures of the ancient Mediterranean. Until quite recently, historians have assumed that the ancient fisheries were of minimal importance, technology was simple and nets were cast from the shoreline. A full reversal of this perception was only achieved as a result of an analysis of the historical evidence matched by an understanding of modern impact studies of pre-industrial fisheries technology. The ancient Greeks and Romans went to sea to fish with hook-and-line as well as nets. Ancient technology was neither ineffective nor unproductive, and indeed produced such large catches that transport, preservation and storage became the limiting factors. One solution to the problem of conserving the fish was to dry and salt it. The most spectacular solution, however, was the reduction of fish to fish sauce – garum – essentially by fermenting the catch in large vats to produce a liquid which was traded all over the Roman world to add flavour to the Roman cuisine. The largest production installations were located near the Straits of Gibraltar and on the northern shore of the Black Sea. The largest installation in present-day Mauretania had a capacity of over 1,000 cubic metres of fish sauce. The fishing industries in the Mediterranean and Black Seas collapsed in the early medieval period and heavy fishing only commenced in early modern times. The seas have been heavily fished through the last few hundred years and ecosystems have been modified dramatically by human interventions. History projects have reconstructed the dynamics of marine animal population in the Venetian Lagoon and in the Northern Adriatic Sea from the 12th century up to the 21st century from historical and scientific sources. A study of the Catalan Sea showed that the impact of modern trawling in the 20th century was particularly severe. Large parts of the Mediterranean and Black Seas are heavily fished down and we are only now beginning to realise the immensity of change and loss.

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A couple of hundred bluefin tuna for sale in the fish auction hall, Skagen, Denmark. Year not stated but no later than 1946. Source: H. Blegvad, 1946.

Fishing in the Gulf of Riga, early 20th century. Image courtesy of Schneider, 1914.

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20TH CENTURY – THE BALTIC SEA One of the early research questions posed by HMAP researchers concerned the eastern Baltic cod population. In the absence of historical records for the period before 1966, they wondered if the record high cod stock in the Baltic Sea in the late 1970s and early 1980s was a unique occurrence or likely to occur at regular intervals. The question was unequivocally answered by the work of the Baltic team. Through the recovery of historical data going back to 1925, we now know that abundant cod stock corresponded to a favourable combination of four key drivers in the late 1970s: incursions of saline water to the brackish Baltic and hydrographic conditions allowing successful reproduction of cod; low marine mammal predation; high productivity environment fuelled by nutrient loading; and reduced fishing pressure. A similar situation did not occur at any other time in the 20th century. The cod biomass in the 1920s-1940s was likely restricted by high abundance of marine mammals and low ecosystem productivity, and in the 1950s-1960s by high fishing pressure. Deteriorating hydrographic conditions have been pronounced since the late 1980s, thereby restricting cod recruitment. Today, cod rarely ventures into the northern Baltic waters between Stockholm (Sweden) and Saaremaa Island (Estonia). During much earlier times, in the late 16th and the early 17th centuries, the presence of a large cod fishery off southern Finland indicates that cod must have been abundant in the northern Baltic. The abundance is all the more remarkable because the population of top predators, such as seals, would have been much larger than it is today, with the ecosystem being oligotrophic. WHEN A SPECIES DECLINES AND

RECOVERS – THE NORTH SEA The first evidence of total removals from the North and Baltic Seas comes from the Danish inshore fisheries in Scania and Bohuslen for herring in the 16th century. By then annual catches regularly reached a level of 35,000 tonnes. By the late 16th century, the Dutch had taken the lead in Northern European herring fisheries with sea-going buysen which harvested the rich schools off the coasts of Scottish mainland and the Orkneys. Total catches with English, Scottish and Norwegian landings amounted to upwards of 100,000 tonnes. Catches declined to about half of that level by 1700, and only increased to about 200,000 tonnes in the late 18th century due to

Swedish and Scottish participation. By 1870 total removals reached a level of 300,000 tonnes, which equals the recommended Total Allowable Catch for 2007 for herring in the North Sea (ICES 2006). This evidence demonstrates how fishermen in the age before steam and trawl were able to remove large quantities of biomass from the sea. The technologies of wind power and driftnets were practically unchanged in the Dutch fisheries from the 16th to the 19th centuries. In the 20th century total catches repeatedly amounted to well over a million tonnes annually, causing collapses of herring stocks and the closure of fisheries for one or two decades to allow populations to rebuild.

COD AND HADDOCK Catches of cod and haddock were abundant in the second half of the 19th century while the stocks showed signs of depletion by the First World War. Detailed historical data are available from the Swedish fishery in the north-eastern North Sea and Skagerrak, which make up about one sixth of the entire North Sea. From these data the minimum total biomass of cod in 1872 has been estimated at about 47,000 tonnes for this portion of the North Sea, but it may have been much higher, while the total biomass of ling was estimated at a total of 48,000 tonnes. These were very healthy stocks if the levels are compared with the modern biomass estimate for cod of 46,000 tonnes for the entire North Sea, Skagerrak and Eastern Channel. For ling no biomass estimate is available as the species is caught too infrequently. EXTIRPATIONS IN THE NORTH SEA Few marine animals have gone extinct in the last few thousand years when human hunting and fisheries may have contributed to species depletion. The fact that few marine species have gone completely extinct is no doubt related to the fact that human activities on the global scale have been restricted to nearshore and midwater realms until the last half of the 20th century. However, human activities, including extraction and disturbance, have spanned the entire North Sea since at least about 800 AD when Vikings were noted to have made a direct crossing of the North Sea from Scandinavia to Northumbria, “something never thought possible before,” according to Bishop Alcuin.

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Fisheries in the Gulf of Riga, early 20th century. Image courtesy of Schneider, 1914.

Fisheries in the Gulf of Riga, early 20thcentury. Image courtesy of Schneider, 1914.

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Pelicans disappeared from the Wadden Sea region of the southern North Sea about 2,000 years ago but the cause of their disappearance is not known. The Atlantic Gray Whale went extinct not only from the North Sea but as a species sometime in the late medieval period, and we may suspect human hunting and disturbance practices to have contributed to the decline of the species, but we have no direct evidence to substantiate the claim. The disappearance of the Great Auk, on the other hand, was certainly caused by widespread slaughter of the flightless bird on the coasts of the North Sea and North Atlantic. The bird disappeared from the North Sea in the Late Middle Ages and the last birds were killed on St Kilda in 1840, in Iceland in 1844 and in South West Greenland the same year. While species extinction is rare in the marine realm, a number of species have been so much reduced in numbers that they are considered regionally extinct or at least so rare that they have lost their ecosystem importance, and their previous commercial importance to the human economy. Regional extinctions have occurred mainly in the late 19th and 20th centuries. Sturgeon was previously caught in vast quantities and marketed in their hundreds at the Hamburg fish auction, for instance. By 1900, however, the fishing declined rapidly both due to river and inshore pollution and to fisheries. As late as the 1930s sturgeon was still caught regularly in the northern Danish part of the Wadden Sea but is now extremely rare. While the sturgeon was easily caught by nets, the blue-fin tuna escaped human hunting activity until the 20th century due to its rapidity and superior strength which made the catch impossible. By the 1920s superior hook-and-line technology was available and brought tuna within the reach of fishermen. Even more importantly, harpoon rifles were deployed in the 1930s and rapidly increased catches to thousands of individuals per year. By 1950, however, tuna catches dropped, and ceased to be of commercial importance after 1955. Climate change and prey abundance seem unlikely causes for the sudden decline, and it now seems possible that the commercial extinction of blue-fin tuna from the North Sea was caused by the heavy onslaught by humans in the mid-20th century. In the southern North Sea, the haddock fishery was of substantial size in the 16th and first half of the 17th centuries. The fishery declined in the later 17th into the 18th century but by the

1770s was on the increase again. We have evidence of an abundant haddock fishery by German and Danish hand liners in the German Bight and up along the Jutland coast in the late 18th century and first half of the 19th. Statistics show substantial catches by 1875, which declined rapidly in the last quarter of the century to nil around 1910. It would seem that the southern North Sea haddock stocks were rendered commercially extinct by the intensive German and Fanø-Hjerting fisheries of the late 19th century. Today, haddock is prevalent mainly in the northernmost part of the North Sea and in the Skagerrak, while its former widespread presence in the southern part of the North Sea was not recognized by marine science until recently.

PUBLICATIONS HMAP research has been published in more than 200 books and papers. Publications can be accessed through several databases:

• For identifying publications concerning a specific marine area visit the HMAP website and look at the dedicated project webpage. Here, all the publications regarding the area are listed along with the contact information for the project leader. www.hmapcoml.org

• At the CoML Bibliographic Database,

all the HMAP publications are listed and searchable by all criteria. http://db.coml.org/comlrefbase

• HMAP Data Pages. By the end of

2010 the data pages will contain more than 1,000,000 data extracted from the HMAP project. The data are online and freely accessible. The HMAP Data Pages are a research resource. www.hull.ac.uk/hmap

• Historical Atlas of Marine Ecosystems

HMAP has developed a dynamic, online historical atlas of marine ecosystems. Using Google Earth and Open Layers, HMAP collects information from historians, ecologists, archaeologists and fishermen to map how marine life and ecosystems in the oceans have changed over time. http://hmap.unh.edu.

Website: www.hmapcoml.org

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Species Abundance, Diversity, Distribution

CHALLENGES TO STUDYING MARINE DIVERSITY

One of the historic challenges in marine biology has been to understand why marine organisms live where they do. Anyone who has been to the seaside has probably noticed that different areas of the sea have different characteristics – here a shallow sandy bottom, there a muddy, silty plain. Of course, in the Northeast Atlantic there is a myriad of different environments where life flourishes, and the physical characteristics are not just constrained to the sediment type (sandy or muddy), but include among many others depth, temperature, food availability and latitude.

CRADLE OF EUROPEAN DEEP WATER RESEARCH

The Northeast Atlantic has been seen as the cradle of deep sea research, due to its accessibility to the early marine research laboratories established in the 19th century. Many of these laboratories and learned societies established surveys of the bottom-living (benthic) animals by sampling along depth gradients, often beginning in the shallow coastal margins and continuing down the continental slope to the abyssal plains below. Recent projects such as MarBEF, Census and EuroCoML have analysed very large data sets of benthic animals to attempt to answer some fairly fundamental questions on the distribution of marine animals, such as: does biodiversity increase or decrease in benthic animals with increasing latitude; does diversity decrease or increase with depth; and what are the other important factors controlling benthic distribution and abundance across this huge area. At the heart of these seemingly simple questions, however, lie some basic disagreements among scientists on how to actually measure diversity. For simplicity’s sake, diversity can be thought of as the number of species present; when comparing samples from different surveys taken with different gear, a more complex index such as Hurlbert’s Rarefaction can be used, which predicts how many species will be present for a given number of individual animals in a sample.

LATITUDINAL SPECIES DIVERSITY GRADIENTS

The data sets examined from the Northeast Atlantic contain around 10,000 species, which allows scientists to test their hypotheses on diversity. For questions related to definable geographical areas of the ocean, some groups such as polychaete worms are more useful than others, as they can be found across all of the areas, perform a number of different ecological functions, and have a variety of different feeding types and lifestyles. One question is known as the Latitudinal Species Diversity Gradient (LSDG): this postulates that there should be a decrease in the number of species with increasing latitude. Using the Macroben data base, no such northward decrease in diversity could be found in the deep sea, once factors such as depth and sampling effort were accounted for. This finding is surprising, as intuitively one might expect the more northerly European seas to resemble more closely the relatively species-poor Arctic Ocean. The highest species diversity occurs in the Norwegian and Barents Seas, possibly because of the influence of warm water currents from the Gulf Stream system bringing water and organisms from the North Atlantic. On a regional scale, the North Sea would appear to show an actual increase in diversity with increase in latitude; the shallow, sandy, heavily trawled southern North Sea is markedly less diverse than the deeper, siltier, less intensively fished northern part. There are, however, so many physical differences between the southern and northern North Sea that saying the difference in diversity may be caused by the change in latitude is almost irrelevant: there appear to be so many other factors at play in determining why diversity is greater in different areas of the North Sea. While there may be no noticeable LSDG in the deep Northeast Atlantic among polychaete worms, some taxonomic groups such as foraminiferans and molluscs have shown such a gradient. Other groups such as nematode worms indicate greater species richness with increasing latitude. What is clear from these particular studies is that different physical factors play diverse roles in structuring where

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Snakelocks anemone found in the Mediterranean. Image courtesy of H. Brown.

Blue shark. Image courtesy of J. Stafford-Deitsch.

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certain groups of animals live. Also, scientific surveys of these remote environments over the years have not used a standardised method of collecting samples, using different sized sieve meshes to separate animals from sediment, as well as using various coring and grabbing devices with different sampling efficiencies, as well as sampling across a wide range of habitats. All of these factors contribute to the lack of definitive answers to questions of diversity gradients and latitude.

CHANGES IN FAUNAL DISTRIBUTION

In the early days of marine science it was thought that because fewer and fewer animals were collected the deeper one sampled, there was a depth at which all life ceased to exist. Although we now know this is not the case, many studies have noted that diversity does change with depth. It is probably not increasing pressure that is the cause of depth distributions (pressure increases with depth), but more likely factors related to temperature, both absolute and range, that are affecting animal distributions. Using the North Sea data set mentioned above, a relationship was found between diversity and depth – the greater the depth, the more species present. In the case of the North Sea, this might be due to the greater temperature range experienced in the southern North Sea, which could be preventing more northern species from surviving the higher summer water temperatures. Away from the relatively shallow North Sea, the Northeast Atlantic continental slope regions generally show an increase in diversity down to 200 metre depth. Below that depth, the number of species present generally declines to a depth of around 500 metres. In the deep Northeast Atlantic it is generally assumed that diversity of large (macrofaunal) animals increases until some intermediate depth, and then gradually decreases again without ever reaching zero; this relationship is parabolic in shape. CHANGES IN SPECIES DIVERSITY

Some of the diversity patterns that were examined for the Northeast Atlantic, North Sea and European Arctic above have also been investigated in other European seas such as the Mediterranean and the Baltic. The Mediterranean allows for such comparisons as it encompasses many habitats and depths in

excess of 4,000 metres. Generally speaking, in the eastern and western basins of the Mediterranean, diversity decreases with depth among most animal groups apart from the single celled microorganisms (Archaea and bacteria). While there are a high number of endemic species in the Mediterranean (around 27%), most of these occur in the shallow coastal margins; the deep Mediterranean is relatively poorly studied and abundances here are very low. In contrast, the Baltic is a shallow, brackish sea. With an average depth of 60 metres, the Baltic only reaches 460 metres at its deepest. While there are roughly 6,000 species in total inhabiting the Baltic, fewer than 1,500 of these are benthic macrofauna. The main factors influencing the distribution of marine life in the Baltic are temperature, salinity and oxygen depletion; the Baltic is strongly stratified, with only periodic inflow of sea water from the western entrance (the Kattegat), and ice cover extends in the shallower areas from November until mid-May.

FACTORS INFLUENCING DISTRIBUTION AND DIVERSITY

As we have seen, there are a number of natural physical factors influencing the distribution and diversity of marine life in European seas. In addition to these factors, man-made or anthropogenic pressures have also played a role; industrial activity, excessive nutrient input and fishing (especially bottom trawling) have all had large impacts on marine life. For example, parts of the southern North Sea are fished 5-10 times per year; some species such as the common skate have been fished to extinction in parts of their former range. In the future we will see greater impacts from pollution and eutrophication as well as from changes in the climate. All of these factors together will no doubt have a major influence on the diversity, distribution and abundance of life in the oceans.

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Pilot whales. Image courtesy of J. Stafford-Deitsch.

Brittle star found on Hatton Bank in the NE Atlantic. Image courtesy of Department for Business, Innovation and Skills (formerly DTI).

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Zooming in on the Detail: Habitat Complexity and Heterogeneity in

European Seas

The ‘habitat heterogeneity’ is one of the cornerstones of ecology. It assumes that structurally complex habitats may provide more niches and diverse ways of exploiting the environmental resources and thus increase species diversity. In terrestrial habitats, plant communities determine the physical structure of the environment, and therefore, have a considerable influence on the distributions and interactions of animal species. In the marine environment, with the exception of very shallow systems, the animal species together with the geological complexity of the seafloor are the main source of heterogeneity and determine the complexity of the habitat. Deep-sea ecosystems represent the large biome of the biosphere but, due to their remoteness are extremely difficult to explore. It is known that shallow water ecosystems are characterized by an extremely structural complexity and habitat heterogeneity. Deep diving is now allowing the direct study of the upper portion of the twilight zone, which is revealing a similar extraordinary diversity of substrates and organisms. The deep-sea floor has long been considered to be a relatively homogeneous environment on a large scale, comprising vast areas of soft surface sediments. Environmental factors, such as food input, hydrodynamics and sediment composition, were assumed to be the main drivers of differences in benthic biodiversity and community composition. Only in the last 20 year has the advent of new, highly sophisticated technology allowed us to investigate these systems in detail and to shed light on the dark portion of the biosphere. As a result of increasing exploration by means of bathymetric and visual mapping of habitats there is now a growing awareness of the true extent of habitat heterogeneity and associated biodiversity along continental margins and abyssal plains. Knowledge of the biological communities associated with, in particular, locally restricted habitats in the deep sea, is increasing and we now have an understanding of how several variables such as substrate availability and type, biogeochemistry, nutrient input, productivity, hydrological conditions and catastrophic events shape patterns of diversity on regional scale. With greater accessibility of remotely operated vehicles (ROV), there has been increasing interest in some deep-sea environments, such

as cold seeps, hydrothermal vents, cold water corals, canyons and nodule areas. This has resulted in an unprecedented direct sampling of these different habitats, which, was often not possible using traditional remote coring techniques. Such studies have shown that they are occupied by benthic communities that are different from those living in surrounding areas of typical deep-sea floor. Recent studies have revealed that, conversely to what was hypothesised, deep-sea ecosystems are not homogeneous, and include a highly heterogeneous mosaic of habitats. Continental margin ecosystems such as coral mounds, canyons or cold seeps can be distinguished from the open slope by their imprints on a topographic map or sonar imagery. These habitats are fundamental for explaining the high biodiversity observed in the deep-sea systems and to the production of fisheries, energy and mineral resources, as well as the critical ecological service of carbon sequestration. The complexity of the life forms, including ‘ecosystem engineers’ able to create hard structures such as carbonate reefs, pinnacles, tunnels etc. along with the erosive effect of bottom currents, sediment diagenesis and tectonic activity create a multitude of habitats only recently recognized as entities that support distinct communities and life forms. The characterization of habitats within these ecosystems requires sampling and/or visual observations. Patterns of species distribution evaluated in the context of relatively monotonous slopes and abyssal plains must now be re-evaluated in the light of this newly recognized habitat heterogeneity.

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The extraordinary architectonic complexity generated by a gorgonian field in the twilight zone of the Calabrian margin. Project Mo-Bio:Mar-Cal, image courtesy of S. Greco, ISPRA. The arm of a Remotely Operated Vehicle (ROV) collecting holothurians from the deep-sea floor of the Atlantic Ocean. Projects HERMES and HERMIONE, image courtesy of NOCS.

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From lush canyons and seamounts, to high-stress oxygen minimum zones and methane seeps, to vast reefs of sponges and corals, the complex linkages between habitat heterogeneity and high biodiversity are

becoming increasingly clear. The deep continental margins (extending from shelf break down to continental rise) are heterogeneous at multiple spatial and temporal scales. These scales interact in complex ways.

A conceptual landscape of the sources of habitat heterogeneity in the deep sea is illustrated on p.27, where the main types of ecosystems are depicted. These include: canyons (1), deep-water corals (2) and coral mounds, seamounts (3), cold seeps and mud volcanoes (4-5), landslides and stable slopes (6-7), hydrothermal vents (8), deep basin (9) and the extreme complexity of the sub-habitats (10). In addition, in the also Oxygen Minimum Zones and anoxic systems can be found in the deep sea. Here we will provide a brief outline of the main deep-sea habitats and their biodiversity. Slopes: The continental slope represents the connection between the shelf and basin plain. Submarine canyons: major topographic systems that incise the continental slope and form part of the drainage system of the continental margins. Seamounts: underwater mountains that do not reach the surface of the ocean. Deep water corals: a deep-water coral reef which stems from a local seafloor mound and consists of accumulations of coral debris, fine- and coarse-grained sediments, and live coral colonies. Hydrothermal vents: vents are created by the emission of hot gas and fluids from the Earth’s mantle. These are generally found near volcanically active places, where they can be quite numerous. Cold seeps: unique systems characterised by the key role of chemosynthesis in the autochthonous production of organic matter. Abyssal Plains: this landscape appears flat and homogenous, but in reality is characterized by the presence of seafloor features up to 35 metres in height. Oxygen Minimum Zones (OMZs): these are bodies of water where dissolved oxygen concentrations fall below 0.5 to 0.2 ml.L-1

Anoxic systems: regions where there is a complete lack of oxygen.

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SLOPES Slopes are by far the most widespread system present along continental margins. The steepness of the slope allows the distinction between progressive, intermediate, and abrupt continental margins. Landslides can shape the seafloor and mobilize huge volumes of sediments. Slopes are ideal systems for investigating benthic biodiversity patterns, as these systems typically show the decrease of benthic abundance and biomass with increasing depth. Open slopes display a benthic species richness similar to, or higher than that reported for bathyal and abyssal plain ecosystems. Biodiversity inhabiting the open slopes reflects a mosaic of life, which shows the heterogeneity and complexity of the substrate. The open slopes are typically composed by soft sediments where communities rely upon particulate organic matter inputs derived from surface production and shelf export. Local-scale sources of heterogeneity are mainly driven by biological activities. Bioturbation, for example, creates micro-topographic features that interact with bottom currents to patchily distribute food on the seafloor.

CANYONS

Submarine canyons enhance the heterogeneity of continental slopes. Their cross sections tend to be V-shaped. Complex canyon networks (e.g. the Gulf of Lions) are sometimes adjacent to sections of the margin with only linear canyons (e.g. the Catalonia margin), or no canyons at all (e.g. the North Balearic margin). They represent hot spots of species diversity and endemism and are

preferential areas for the recruitment of megafaunal species. Canyons probably play an important role in structuring the populations and life cycles of planktonic fauna, as well as benthic megafauna fishery resources that are associated with them. For example, canyons are important habitats for fished species, such as hake (Merluccius merluccius) and for the rose shrimp Aristeus antennatus. Because of their characteristics, the biodiversity of faunal assemblages can be markedly different from that on the adjacent open slopes.

A gorgonian field along the southern slopes of the Italian margin. Project Mo-Bio:Mar-Cal, image courtesy of S. Greco, ISPRA

The three pictures illustrate the sessile and mobile fauna on hard bottom of a flank of a deep-sea canyon along the Portuguese margin. Projects HERMES and HERMIONE, image courtesy of NOCS.

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SEAMOUNTS Biogeographically, seamounts are islands separated by great depths. Consequently, they may serve as isolated refuges for relict populations of species that have disappeared from other areas. A complete and detailed map of all seamounts around EU margins is not available yet and biological studies have been very limited. In the Western Mediterranean, the Tyrrhenian bathyal plain is characterized by a large number of seamounts (Magnaghi, Vavilov, and Marsili seamounts) and include crescent-shape bathymetric ridges (horsts) bounded by normal faults (Vercelli and Cassinis ridges). In the Eastern Mediterranean, the Eratosthenes Seamount is an impressive geological structure. Trawl and grab sampling at a depth of 800 metres have revealed a relatively rich and diverse fauna including scleractinian corals (Caryophylla calveri and Desmophyllum dianthus), encrusting poriferans, scyphozoan polyps, actiniarians, bivalves, sipunculides, asteroids and fish. The seamounts also have an effect on the biodiversity of surrounding sediments and current research in Marsili, Dauno and Vercelli seamounts is providing evidence of a high biodiversity. However, most of the EU seamounts remain largely unexplored, and much work is needed to discover the potential contribution of these systems.

The three pictures illustrate the extreme variability of the habitats that can be encountered along the profile of a seamount. Top and middle images courtesy of S. Greco, ISPRA; bottom image courtesy of NOCS.

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DEEP-WATER CORAL ECOSYSTEMS

These coral ecosystems represent an extremely complex and heterogeneous substrate, providing additional hard substrate. These reefs form locally elevated hard substrates associated with strong bottom currents that enhance food supply. The colonial stone corals Lophelia pertusa and Madrepora oculata which occur along the northwestern European continental margin and the deep shelves and in Scandinavian fjords (often associated with Corallium rubrum and gorgonians, e.g. in the Mediterranean Sea), are also present in different sectors of the deep Mediterranean Sea. Some of the solitary species, such as Desmophyllum dianthus, also contribute to the reef frameworks. The presence of these banks in the warm deep Mediterranean is intriguing as these systems are known to occur in cold water systems and it is possible that in the Mediterranean these species are at the threshold level of their tolerance to high temperatures and M. oculata and L. Pertusa could be relicts of a much more extensive distribution during the Pleistocene. At present, a total of 14 coral bank areas have been identified, but only a few of them have been examined by ROV dives from the Gibraltar sill to the Gulf of Lions canyons, from the Ligurian Sea to the Sicilian Channel, and from the Apulian margin to the trough off Tassos in the Aegean Sea. The depth distribution of the corals ranges from 150 metres down to bathayl/abyssal depths. Deep-water corals generally occur along the edge of the continental shelf, on offshore submarine banks and in canyons. A huge number of species is associated to these coral banks, this number depends on the system and geographic location but can easily be over 222 species. These species that include the most diverse taxa were Porifera, Mollusca, Cnidaria, Annelida, Crustacea, brachiopods, echinoderms, Bryozoa and fish (including the deep-water shark Etmopterus spinax). Several gorgonians such as Bebryce mollis, Swiftia pallida and Paramuricea macrospina can be associated with these systems. Most of the species are boreal and cosmopolitan. Interestingly, a very high biodiversity of the infauna is also associated with the coral rubbles (detritus and fragments of dead corals), which are present around living coral areas or in fossil systems. Coral mounds are topographic highs build up by the accretion of hard colonial corals and sediments developing into a complex three-dimensional structure. The largest coral mound reported so far is the

Røst reef off Norway, spanning an area approximately 40 kilometres long by 3 kilometres wide. In these environments, structural complexity is a major source of heterogeneity. The occurrence of living and dead founding species, which determines biotic interactions like competition, predation or chemical defences also play an important role in habitat partitioning.

An example of the extreme complexity of the deep-water coral habitats that can be encountered along the European margins. Images courtesy of Department for Business, Innovation and Skills (formerly DTI).

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HYDROTHERMAL VENTS

Deep-sea hydrothermal vents typically form black smokers and are biologically more productive, often hosting complex communities fuelled by the chemicals dissolved in the vent fluids. In the last decade, the discovery of an extensive hydrothermal field at 30 degrees north near the eastern intersection of the Mid-Atlantic Ridge and the Atlantis fracture zone (i.e., the vent field named 'Lost City') opened new scenarios for the exploration of these systems not only along mid-ocean ridges but also on old regions of the oceanic crust away from spreading centres. In hydrothermal vents chemosynthetic Archaea form the base of the food chain, supporting diverse organisms. The fauna of Atlantic vents consists for the most part of a subset of invertebrate types found elsewhere in chemosynthetic ecosystems, with taxonomic differentiation usually at the species or genus level. Despite this similarity in taxonomic composition, the ecology of Atlantic vents differs from the ecology of Pacific vents in ways that highlight aspects of biogeography, trophic ecology and sensory adaptations. While oceanic hydrothermal vents typically occur at depth over 3,000 metres, most hydrothermal vents in the Mediterranean with described biological assemblages occur in shallow depths of less than 100 metres. Consequently, a profound difference between these and the described oceanic deep-sea vents is the occurrence of photosynthetic primary production. Also, the species that inhabit shallow-water Mediterranean hydrothermal vents are not endemic to these habitats but represent a subgroup of the most tolerant species in the ambient fauna. The only published evidence for deep-sea hydrothermalism in the Mediterranean consists of indicators of extinct activity observed on the peak of Marsili Seamount in the Tyrrhenian Basin at about 450–500 metres depth.

COLD SEEPS AND MUD VOLCANOES

C anaerobic methane oxidation coupled with sulphate reduction by chemosynthetic bacteria facilitates the formation of carbonates and may generate extremely high concentrations of hydrogen sulphide in pore waters. The variations in the fluid composition and flow rates have been correlated to many attributes of cold seeps including microbial biogeochemistry, availability of hard substrata by carbonate precipitation, the distribution and

succession of symbiont-bearing bivalves and tube worms, as well as their associated non-chemosymbiotic mega-, macro- and meiofaunal assemblages. Active seepages range in scale from about a 100 square metres to 10 square kilometres. These systems are known from a wide range of European seas from the Portuguese continental margins to the Nordic margin, from the Mediterranean Sea to the Celtic margin, at depths from a few hundred metres to over 4,000 metres. In various cold-seep habitats carbonate crusts and associated fauna were observed down to 2,000 metre depth. Mud volcano fields explored in the Mediterranean (Napoli, Milano, Urania, Maidstone mud volcanoes) displayed the presence of brines. Submersible dives allowed identifying large fields of small bivalves, large siboglinid tube worms, large sponges, and associated endemic fauna. Several species of bivalves harbouring bacterial symbionts colonize methane- and sulfide-rich environments. A new species of Siboglinidae polychaete, the tubeworm colonizing cold seeps from the Mediterranean ridge to the Nile deep-sea fan, has been recently described. An exceptional diversity of Bacteria lives in symbiosis with small Mytilidae. The Mediterranean seeps appear to represent a rich habitat characterized by megafaunal species richness (e.g. gastropods) or the exceptional size of some species such as sponges (Rhizaxinella pyrifera) and crabs (Chaceon mediterraneus), compared with their background counterparts. The isolation of the Mediterranean seeps from the Atlantic Ocean after the Messinian crisis led to the development of unique communities, which are likely to differ in composition and structure from those in the Atlantic Ocean.

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Cold seeps are also inhabited by rich assemblages associated with either soft sediments influenced by cold seep emissions and carbonate crusts. Images courtesy of M. Sibuet and J.P. Foucher, IFREMER.

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ABYSSAL PLAINS The abyssal plains of the European Seas occur typically at depths ranging from approximately 3,000 metres (in the Mediterranean Sea) to 5,000 metres (in the Atlantic Ocean). Sediments filling the abyssal plains are generally dominated by the deposition of turbidities. These landscapes are only apparently flat and homogeneous, but instead are characterized by the presence of seafloor features up to 35 metres in height. In addition, biological activities, bioturbation and excavation by infaunal organisms, as well as the deposition of organic debris and cadavers of pelagic organisms can produce a large spatial and temporal heterogeneity at different spatial scales. Typical deep-water groups include large species contributing to spatial heterogeneity at small scale, such as echinoderms, glass sponges, and macroscopic Foraminifera (Xenophyophora). Fishes, decapod crustaceans, mysids, and gastropods are widespread, although much less abundant in the deep Mediterranean than in the northeastern Atlantic.

OXYGEN MINIMUM ZONES The Oxygen Minimum Zones (OMZs) are bodies of water where dissolved oxygen concentrations fall below 0.5 to 0.2 ml.L-1. Where an OMZ impinges on the seafloor, hypoxia profoundly modifies the structure of benthic communities over areas ranging from 8,000 square kilometres up to 285,000 square kilometres. At such large scales, many factors can interplay to structure benthic communities but the availability of oxygen is likely the most important one. OMZs are systems that typically have low levels of biodiversity. Very few are found in European waters, however hypoxic systems are more frequently found, especially in the northern Adriatic Sea or Baltic Sea. These systems are not widespread in the European deep-sea.

ANOXIC SYSTEMS Numerous deep hypersaline anoxic basins (DHABs) have been discovered in the Eastern Mediterranean Sea, the Red Sea, and the Gulf of Mexico. The six DHABs of the Eastern Mediterranean (L'Atalante, Urania, Bannock, Discovery, Tyro, and La Medee) are located on the Mediterranean Ridge. These anoxic basins lie at depths ranging from 3,200 metres to 3,600 metres and contain brine. The combination of nearly saturated salt concentration and corresponding high density and high hydrostatic pressure, absence of light, anoxia, and a sharp chemocline makes these basins some of the most extreme habitats on earth. In these basins a bacterial diversity higher than in the overlying deep seawater can be found. In the Bannock basin, five new candidate divisions were also identified in the seawater-brine interface through clone libraries. The anoxic layers were dominated by Delta- and Epsilon-Proteobacteria. A recent study carried out on the thermal mud fluids of Urania Basin, revealed the presence of a highly diverse prokaryotic community, mostly composed of unculturable prokaryotes. Recently, the first metazoa living in the permanently anoxic conditions were discovered. The sediments of L’Atalante basin were inhabited by three species of the animal phylum Loricifera (Spinoloricus nov. sp., Rugiloricus nov. sp. and Pliciloricus nov. sp.) new to science.

One of the three species of Loricifera

discovered in the anoxic sediments of the L’Atalante basin in the Mediterranean Sea. Image courtesy of R. Danovaro, UNIVPM - CoNISMa

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The apparently homogeneous deep-sea floor is punctuated by a myriad of heterogeneous holes and depressions due to animal reworking of the sediment. Image courtesy of D. Billett, NOCS.

The hard bottoms of deep-sea canyons are also characterised by a high topographic heterogeneity and host a wide variety of species, dominated by sessile suspension feeders. Image courtesy of NOCS.

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SPATIAL SCALES OF HABITAT HETEROGENEITY

Continental margins are characterized by an ample spatial variability at both large scale (among different margins and latitudes), mesoscale (among stable and unstable open slopes, canyons, oxygen minimum zones, cold water corals or seeps) and at small spatial scales (within each habitat type). The patterns of biodiversity and species turnover can be, at least partly, related to habitat heterogeneity at regional and large spatial scale. If the information available on biodiversity patterns at large spatial scales is still limited, the knowledge of the patterns at regional to small spatial scale is not much more advanced. The quantification of habitat and sub-habitat heterogeneity in deep sea is not an easy task. Even in terrestrial ecology, only few attempts have been made to propose widely-used metrics. In a large landscape of a continental margin, structural richness (i.e. the number of habitats) may yield a good insight into the relationship between habitat heterogeneity and species diversity, especially if the habitats are very distinct. Mapping physical structures in a habitat is a tool that can be used in assessing habitat heterogeneity. The quantification of substrate heterogeneity can be obtained from image analysis of digitized bottom photographs at any scale. Image analysis allows the evaluation of substrate heterogeneity metrics such as the composition and spatial configuration of substrate patches, for instance. A recently developed method of remote habitat mapping employs processed multi-beam backscatter data to generate important information about bottom heterogeneity (e.g. rugosity, slope, hardness, etc). For instance, in habitat created by ecosystem engineers (corals, sponge fields and oyster banks) or in chemosynthetic systems (seepage), the heterogeneity at small spatial scales can be crucial for promoting high levels of biodiversity, thus enhancing ecosystem functioning. This is the case of the seeps in which there are small scale gradients of sulphide availability that create a variety of opportunities. Microhabitat-induced diet and congeners may enhance niche separation by diet distinction thus influencing biodiversity and the efficiency by which available resources are utilized.

Zooming at a smaller spatial scale a large heterogeneity can be found not only on hard bottom but also on soft substrates. Top and middle images courtesy of ISPRA; bottom image courtesy of NOCS

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PRESERVING HABITAT DIVERSITY AND HETEROGENEITY

Hot-spot ecosystems are typically characterized by high habitat/topographic complexity. These hot spots, bearing a higher biodiversity than other deep-sea ecosystems, typically support higher levels of ecosystem functioning and efficiency. Since most of the seafloor is still unexplored, while anthropogenic impacts leading to habitat destruction or homogenization (e.g. trawling) are extending even to the most remote marine

regions, action is needed now to preserve biodiversity before that this is lost. A possible solution for the conservation of the hot spots of biodiversity is applying the precautionary principle to protect the deep-sea areas around EU margins and islands that are topographically highly complex and heterogeneous. This action would be certainly beneficial for preserving the associated biodiversity and is extremely important for the sustainability of deep-sea ecosystem processes.

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Biodiversity in European Seas

CUMULATIVE KNOWLEDGE The study of marine biology has a long history in Europe and the diversity of marine organisms is probably more comprehensively documented for European waters than anywhere else on Earth. After well over two centuries of detailed exploration we know, with a high degree of accuracy, that in the year 2000 at least 29,714 species of marine organisms had been recorded from European seas. Almost all animal phyla occur in the oceans, so diversity in basic body organization is high, but species richness is not evenly spread across all marine groups. The top dozen dominant taxa in Europe comprise over 25,500 species, over 85% of the total (p.39). The largest taxon is the Crustacea which, with 7,137 European marine species, is more than twice the size of the next most species rich group, the Mollusca, with 3,353 species. The next three groups are all worms of different kinds. The flatworms comprise the third largest taxon within the European marine fauna with 2,398 species. Over half of them are parasites, either gill flukes (Monogenea) or intestinal flukes (Digenea), or tapeworms (Cestoda). Next are the annelids (2,160 species), comprising the free-living polychaetes and oligochaetes, plus the leeches. Then we have the nematodes. Free-living nematodes are both abundant and species rich, but the diversity of marine benthic nematodes is poorly represented in checklists since only a small proportion of the estimated total number of species has been described and named. Parasitic nematodes are common in marine metazoan hosts but comprise a relatively small part (12%) of total nematode count (1,837 species) in European seas. The macroalgae are the sixth most abundant group, although this grouping is an artificial assemblage of red, brown and green algae. They are followed by the sponges (1,640 species) and then the fish (1,349 species) and cnidarians (1,329 species). In the eighth place are the foraminiferans (1,167 species), followed by the Bryozoa (724 species) and the dinoflagellates (718 species). Just dropping out of the top 12 are familiar but relatively low diversity groups such as the echinoderms (648 species) and the tunicates (481 species).

The discovery of new marine organisms continues apace – with an average of about 1,500 new species described globally each year over the past 20 years. These range from microbial end of the size spectrum, such as Archaea and bacteria, up to vertebrates, but the great majority of newly described species comprises multi-cellular invertebrates. Although European waters are relatively well studied, new species are continually being recognised there: since 2000, species new to science have been added to the European Register of Marine Species (www.marinespecies.org) at a rate of just over 50 per year. Including the species described that originate from outside of Europe but have either been found in, or have spread into, European waters in the past decade, adds further to the regional fauna. The total number of marine species for Europe is now approaching 32,000 and represents nearly 14% of global marine diversity, estimated by Bouchet as approximately 230,000 species.

NEW MICROBES The discovery of new species is often dependent on the use of new technology or new investigation tools. This is especially true of the microbes which can be extremely abundant, with one million bacteria in a single one millilitre drop of sea water, and can exhibit high diversity, with up to 10,000 bacterial species per millilitre. Since scientists cannot identify most microbes by their external appearance, they have to rely on molecular methodologies to describe their diversity. A standard method is to study the ribosomal genes, in particular the so-called 16S and 18S ribosomal ribonucleic acid genes, which are extremely stable gene subunits, providing information that corrupts only slowly through geological time scales. Determining the genetic code (the base sequences) in these genes provides insight into the evolutionary relationships and therefore the classification of the organism, as well as insight into its functional properties. The red bacterium Rhodopirellula baltica (p.39) was originally isolated from the Baltic Sea but was thought to occur widely in the seas around Europe. However,

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Crustacea Mollusca Platyhelminthes AnnelidaNematoda Macro-algae Porifera FishCnidaria Foraminifera Bryozoa Dinoflagellates

The dozen most diverse groups of marine organisms in European seas

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Cells of the planctomycete bacterium Rhodopirellula baltica (A). Colonies of the Rhodopirellula baltica isolated from the bay of Kiel (B). Images courtesy of J. Harder.

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characterization of the bacterium on the genetic level, using 16S rRNA, revealed a cluster of species within the genus Rhodopirellula. Using a technique called whole genome hybridization it was shown that Rhodopirellula baltica was actually restricted to the Baltic Sea, the Skagerrak and the eastern North Sea. The majority of the isolates obtained belonged to a second species present in the English Channel, on the French Atlantic coast, and in the Mediterranean. A third species was found in North Atlantic habitats around Iceland and Scotland and a fourth species in the Adriatic Sea. The presence of four species of Rhodopirellula in European seas shows considerable evolutionary diversification within the genus. Rhodopirellula baltica was the first planctomycete bacterium to have its genome completely sequenced, and transcriptional profiling confirmed that R. baltica is highly responsive to changes in its environment. This makes R. baltica ideal to serve as a model organism, but only if the species is correctly identified.

NEW INVERTEBRATES Higher up the size spectrum are the copepods - diminutive relatives of the crabs and lobsters, but abundant and diverse in the oceans. There are about 3,000 species of copepods in European waters, and they comprise about 10% of all species contained in the European Register of Marine Species. Free-living copepods are typically the dominant group of multi-cellular animals in the plankton but they also live on and in marine sediments where they are usually second in abundance only to the nematodes. Copepods are also parasitic on hosts representing almost every phylum from sponges to chordates, including whales. Several families are parasitic on polychaete worms but these parasites are typically rare and our knowledge of their biology and distribution has been extremely limited. Such parasites are usually found by researchers studying the hosts so the sheer amount of macrobenthic sampling and analysis that has taken place within the past decade has provided an exciting opportunity to collect these very rare animals. The diversity of new forms found was astonishing: in a large series of samples taken from around the Norwegian Sea and White Sea, a total of 11 species new to science and three new genera of copepods were identified. The numerous new host and geographical records have greatly improved

our knowledge of the host specificity of the parasites, their abundance, and their distribution in European waters. There is even an as yet unnamed new parasitic copepod (p.41) which lives on the sabellid polychaete Jasmineira caudata. The copepod body is transformed into a globular trunk which carries egg sacs, but its anterior end penetrates the body wall of its host. The unusual features of this parasite exclude it from all known families and it may represent an entirely new family from European waters. One of the generally under-explored sectors of multi-cellular animal diversity is the parasites. Marine fishes serve as both intermediate and final hosts to a wide diversity of flatworm and other parasites in European waters and the fauna remains incompletely known, especially in deep water. Specimens of the short-fin spiny eel Notacanthus bonaparte caught at depths in excess of 1,000 metres on the Goban Spur had intestinal flukes which were described as a new genus and species of digenetic fluke, Steringovermes notacanthi, by Bray. Many digeneans are specific in their choice of host and Steringovermes notacanthi is named after its notacanthid host. Invertebrates also have parasites, although less is known about them than parasites of vertebrate hosts. The separate subclass status of microscopic parasites called tantulocarids was first recognised in the 1980s and these parasites continue to be discovered on various marine crustacean hosts in the oceans of the world. They occur throughout European seas but are rarely reported because of their small size. The most recent addition to the fauna is Microdajus tchesunovi from the White Sea, which was described only in 2010. The larval stage of Microdajus is only 100 microns in length and is attached to its tanaid host by means of an adhesive oral sucker (p.41). Newly discovered in European waters is the crustacean subclass Cephalocarida, which have often been considered to be the most known primitive crustaceans. The species, Lightiella magdalenina, was originally known from a very restricted site, about 15–20 metres deep on the southern shore of a tiny island in the La Maddalena Archipelago, off Sardinia, but it has since been found off the coast of Tunisia.

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Scanning electron microscope photograph of a sabellid worm Jasmineira caudate parasitised by two females (top left). Scanning electron microscope photograph of the tanulus larva of Microdajus attached to its tanaid host (top right).

The heart urchin, Echinocardium cordatum, is a complex of five morphologically indistinguishable species. Image found at de.academic.ru/dic.nsf/dewiki/1339925

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GENETIC STUDIES AND CRYPTIC SPECIES

Biodiversity describes the variety of life at all scales from genes to ecosystems and modern molecular genetic methods have enabled us to study fine scale, within-species variation. Such approaches have dramatically improved our knowledge of the complex structure of marine fish populations and their adaptations to environmental gradients and local conditions. This knowledge helps us to analyse the environmental basis for spatial structure in fish populations, and examine how the spatial distribution of local populations changes over time. The new methodologies have been applied to marine species such as cod, herring, and sprat throughout the salinity gradient in the North Sea – Baltic Sea area. These analyses showed that the steepest gradient in genetic variation largely coincided spatially with the steepest gradient in salinity (i.e. in the western Baltic Belt Sea area), and that populations in the Baltic were genetically distinguishable from those in the North Sea. In the case of the sprat, Sprattus sprattus, the existence of isolated genetically distinct populations has been demonstrated in the northern Mediterranean basins and they remain isolated because of their inability to maintain gene flow in the currently warmer oceanographic regime in the Mediterranean. Such advances in knowledge of fish genetics can help improve the way fisheries are managed and inspected, including efforts to prevent illegal fisheries. The genetic analysis of marine organisms has shown various examples of cryptic species, i.e. populations previously thought to belong to the same species because of a lack of morphological diagnostic characters. The heart urchin Echinocardium cordatum, for example, is found from the North Atlantic to the Pacific, including the Mediterranean. Because its development includes a planctotrophic larva stage which confers a high dispersal potential, it has been treated as a single widespread species. Recent genetic studies have shown that E. cordatum (p.41) is a species complex consisting of five different clusters, separated by clear genetic discontinuities which in turn provide strong evidence of reproductive isolation and therefore speciation. Three of these clusters (clades) exist in European waters: one restricted to the Atlantic, a second ranging from the Atlantic off Galicia into the Mediterranean, and a third restricted to the Mediterranean. The other two clades are North and South Pacific.

Two forms of the phyllodocid polychaete Notophyllum foliosum were known to occur in Scandinavian waters. There was a deeper water form that was palish yellow to grey in colour, with black patches, and a shallower form that was yellow-orange with black patches and white spots. The deeper form was often associated with reefs of the deep-water coral Lophelia pertusa. Using two different genes, recent analysis showed that these two forms represent different species and the deeper form was formally named Notophyllum crypticum. The species complexes discovered for Echinocardium cordatum and for Notophyllum are just two examples of the widespread phenomenon of cryptic speciation. Cryptic species can arise when genes and morphology evolve at different rates, so they have undergone rapid genetic evolution leading to reproductive isolation, but this is not reflected in similarly rapid morphological changes. Discovering and documenting this hidden biodiversity is a major challenge for marine biologists.

EXTREME ECOSYSTEMS The exploration of extreme ecosystems, such as marine caves, has provided some notable discoveries. Such caves provide a permanently dark, stable, quiescent environment with limited food resources that offers some parallels with the deep sea. In the north-western Mediterranean one particular cave, the 3PP cave near Marseille, has a descending profile that traps cold water (~13-15°C) all year round and the deep interior of the cave shows strong faunal and ecological parallels to the deep sea. One of the most striking and best studied examples is the carnivorous sponge Asbestopluma hypogea (p.43). This belongs to an exclusively bathyal and abyssal sponge family, the Cladorhizidae, but is found in dense populations at 15-25 m depth in particular caves. The same caves can also harbour the fragile hexactinellid glass sponge Oopsacas minuta, normally found between 300 and 3,000 metres in the deep Mediterranean. These descending cold-water caves are home to an interesting mixed marine cave fauna, successfully established true deep-sea species, and an additional consortium of mobile shallow-water taxa using caves as shelter from predators.

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The carnivorous sponge Asbestopluma hypogea from a cave near Marseille. Image courtesy of P. Chevaldonné.

The frenulate worm Bobmarleya gadensis collected at depth of 2200 metres on the Carlos Riberio mud volcano in the Gulf of Cadiz. Image courtesy of A. Hilário.

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Other extreme habitats that have provided rich sources of new species in recent years include hydrothermal vents, cold seeps, gas hydrates and mud volcanoes. The mud volcanoes in the Gulf of Cádiz, first discovered in 1999, are inhabited chemosynthetically-based communities dominated by frenulate worms (members of the polychaete family Siboglinidae). One new frenulate (p.43) discovered at a depth of 2,200 metres on the

Carlos Ribeiro mud volcano was described by Hilário and Cunha under the name Bobmarleya gadensis. This splendid name pays tribute both to the “shape of the tentacular crown in which tentacles largely resemble dreadlocks, a hairstyle popularised by the reggae singer and songwriter Bob Marley”, and to the proximity of Cádiz (the name of which was Gades in Roman times).

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Alien Species

ORGANISM GROUPS Marine alien species represent extremely broad taxonomic spectrum of aquatic free-living and parasitic organisms, including bacteria, plants, animals, fungi and other organisms. Amongst bacteria, for instance, the Vibrio cholera bacteria has been dispersed by sea going vessels. Amongst plants, green, red and other algae (e.g., diatoms and dinoflagellates); mosses, liverworts and hornworts; and flowering plants have been recorded as alien species. Amongst animals, several representatives of the following taxons have been recorded as aliens: annelids, bony and cartilaginous fish, bryozoans, chaetognaths, cnidarians, crustaceans, echinoderms, insects, molluscs, nematodes, sea squirts and sponges.

INVASION SUCCESS Higher potential to become an alien is shown by species with high abundance in native habitat, ability to survive during the introduction process, wide range of habitat selection, high tolerance to abiotic factors, wide food spectrum, high reproduction rate, fast growth, alien status elsewhere, potential to replace native species, long-lasting larval stage, pelagic life-history stage and ability to produce resting stages. Introduction hot spots are areas with matching hydroclimate (i.e., temperature and salinity) between the destination and source region. In addition, the following characteristics of the destination area are important: availability of ‘ecological niche’, low abundance or absence of predators and parasites, strong anthropogenic influence, low native species diversity.

TERMINOLOGY Non-indigenous (alien, exotic, non-native) species are species or lower taxa introduced outside of their natural range and dispersal potential. This includes any part, gamete or propagule of such species which might survive and subsequently reproduce.

Invasive alien species are a subset of established nonindigenous species which have demonstrated their potential to spread elsewhere and have adverse effect(s) on invaded regions.

Cryptogenic species are those of unknown origin which cannot be defined as being native or alien.

Introduction is either intentional or unintentional human-mediated dispersal of nonindigenous species. Secondary introduction of nonindigenous species from the area(s) of their first arrival could occur without human involvement due to spread by natural means.

Biological pollution (biopollution, bioinvasion impact) is the impact of invasive alien species at the level that disturbs ecological quality by having effects on individual, population, community, habitat and ecosystem levels.

ORIGIN IN EUROPE Non-indigenous marine biota in different European seas originates from diverse source areas. Some species have been introduced from distant overseas regions (e.g. south-eastern Asia, Australia, New Zealand, Americas), while others from one region of Europe to another, i.e. from the Ponto-Caspian region to the Baltic, or from the North Sea to the Black Sea. Generally, the biogeographical composition of alien biota is region-specific: for example, in the Mediterranean Sea most of the alien species originate from tropical areas, mainly from the Red Sea, Indian Ocean or Indo-Pacific, while in the Baltic Sea donor regions such as North America, the Ponto-Caspian region and south-eastern Asia dominate.

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Green macroalgae Caulerpa racemosa var. cylindracea. Image courtesy of M. Cormaci.

Chinese mitten crab Eriocheir sinensis. Image courtesy of Estonian Marine Institute.

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TRANSPORT PATHWAYS (WITH EXAMPLES OF MAIN

VECTORS) • Ships: ballast water and sediments, hull

fouling, intakes and crevices, bored wood, bilges and ships water, anchor and anchor chains, lockers fenders, portable moorings, deck recesses, dredge spoil and sediment displacements;

• Canals: water flow, tidal exchanges, and other alteration to water levels from lock flushing, transport of floating timber, pontoons;

• Wild fisheries: stock movements, population re-establishment, discards, disease agents from fish processing, live bait releases and discharges of live packaging material, movement of retrieved fishing equipment, releases of organisms intended as living food supplements, releases of transported water;

• Culture activities: intentional releases and movement of stock associated water, movement of gear, discarded or lost gear, live packaging materials and/or associated transport media, release of genetically modified species;

• Aquarium and live food trade: intentional and accidental releases from aquaria, untreated waste discharges, unauthorised releases of imported living foods, discharged live packaging materials, releases of transported water;

• Leisure activities: live bait movements, discharge of packaging materials, accidental/ intentional transport and release of angling catch, water sport equipment, stocking for angling;

• Research and education: intentional and accidental release, wastewater and biological waste discharges, discarded samples, releases from cultures, gear movement, releases/ escapes of caged organisms;

• Biological control: releases to control invasive species;

• Habitat management: soil stabilization/reclamation, sediments and plantings, use of filter-feeding invertebrates for managing water quality.

INVASIVE SPECIES The marine fauna of the Eastern Mediterranean is undergoing a profound and rapid change due to sustained immigration of

Red Sea species through the Suez Canal into the Mediterranean (commonly referred to as Lessepsian or Erythrean immigration). Estimates of the number of Erythrean immigrant metazoan species vary from 558 to 903, with the disparity largely due to different authentication protocols between studies. Despite the uncertainty over the precise number of immigrants, the influx continues apace and the scale of the problem has led to the recognition by the European Environment Agency (EEA, 2006) of biological invasions as one of the priority issues of concern to the health of Mediterranean marine ecosystems. Changes to the Eastern Mediterranean fish fauna have been particularly visible and the populations of some immigrant species have grown to the point where commercial fisheries have been established to harvest them. Immigrant species of Red Sea clupeids such as red-eye round herring Etrumeus teres for example, are important in inshore-pelagic fisheries off the Egyptian coast. There have been few studies of the parasites of these immigrant fish, but recently the gill parasitic copepod Mitrapus oblongus has been discovered in the Mediterranean for the first time. This parasite originates in the Indo-Pacific but has been carried into the Mediterranean via the Suez Canal on its Red Sea immigrant host. The alarming discovery here is that Mitrapus oblongus was also found on the gills of a native Mediterranean clupeid fish, the sardine Sardinella aurita. This is the first documented case of host switching of any metazoan parasite from a Red Sea immigrant to a native fish host. The potential impacts of such host switching events on the populations of native hosts are profound, especially when the hosts are the subject of important fisheries. Alarmingly, at least four more Red Sea parasitic copepods have since been found in the eastern Mediterranean.

THREATS AND BENEFITS Invasive alien species might threaten humans, cause adverse effects on environmental quality and cause damage to economies. However, invasion of alien species may also be beneficial to marine ecosystems as well as to goods and services they provide to humans.

Examples of impact to human health: Cholera is one of the best known fatal diseases. Caused by various strains of Vibrio cholera bacteria, symptoms of the disease vary from mild to acute diarrhoea accompanied

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Green macroalgae Codium fragile. Image courtesy of E. Ballesteros.

Pacific oyster Crassostrea gigas. Image courtesy of A. Jelmert.

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by abdominal cramps, nausea, vomiting, dehydration and shock. The planktonic dinoflagellate Alexandrium catenella which occures in several European regional seas, is responsible for creating ‘red tides’ and producing paralytic shellfish poisoning (PSP) toxins which can affect humans, other mammals, birds and fish.

Ecological impacts: Impacts of alien invasive species have been recorded at genetic, species, community and ecosystem levels. These might range from simple interactions between non-native and native species to massive shifts at biotope level resulting in altered ecosystem functioning. Alien invasive species can also act as ecosystem engineers, influencing the habitat itself, positively or negatively, directly or indirectly (see sections on threats and benefits below).

Examples of economic losses: Invasion of alien species may result in significant economic losses for shipping industry, fishery and tourism. In addition, they may cause harm to culture and aesthetic value of oceans. The Ponto-Caspian zebra mussel (Dreissena polymorpha) is perhaps one of the most ’famous’ examples of bioinvasions. It is primarily a freshwater species, but lives in brackish ecosystems. It was unintentionally transported to the North American Laurentian Great Lakes in the 1980s. Since then, and through significant and devastating impacts on several abiotic and biotic ecosystem properties, fishery and infrastructure, the estimated financial damage in the US was up to one billion dollars. The predatory comb jelly (Mnemiopsis leidyi) was accidentally introduced via ship ballast water to the Black Sea in the early 1980s. In its new predator-free habitat, the jellyfish colonised the entire ecosystem and through trophic interraction (by predating on zooplankton, fish eggs and larvae) disrupted the foodweb and contributed to collapse of the local fishery resources with monetary damage of several hundreds millions dollars. The small phytoplankton alga Chattonella cf. verruculosa produces toxin which affects the gill tissue of fish resulting in the production of mucus which makes the fish suffocate. It has been estimated that the fish killed 350 tonnes of farmed Norwegian salmon.

THREATS • Human health; • Changes in resource competition (food,

space, spawning/nursery areas) • Changes in habitat (chemical, such as use

of biocides; physical, such as reduced water movements; biological);

• Limitation of resources (e.g., space, nutrients, light, oxygen);

• Introduction of new functional groups and changed foodwebs;

• Uncontrolled dispersal through unexpected ecophysiological response;

• Introduction of potentially toxin producing species (harmful algal blooms, some seaweeds);

• Introduction of disease agents or parasites (viruses, bacteria, fungi, ecto- and endoparasites) associated with an introduced host species;

• Genetic effects on native species (hybridisation, change in gene pool, loss of native genotypes);

• Reduction or extinction of native populations;

• Alterations of native communities; • Introduction of a species being a missing

link as host in the life cycle of parasite; • Effects on underwater constructions by

fouling alien species (water intakes of power plants and urban water supplies, boats), expensive cleaning procedures and application of preventive measures (antifouling paint);

• Tourism (accumulation on shores causing smell or sharp shells that have to be removed, dense growth in shallow bays used for swimming);

• Loss of commercial or recreational fishery; • Losses of aquaculture harvest; • Cost of chemicals for eradication; • Damage caused to underwater heritage

objects such as sunken sailing vessels; • Shoreline erosion; • Recreational value; • Aesthetic and artistic values. Examples of economic benefits: Alien species may also be economically beneficial. For instance, the red king crab Paralithodes camtschaticus was intentionally transferred from areas in the Northern Pacific Ocean to the Barents Sea in the 1960s as larvae, juveniles and adults. The species now forms new and valuable commercial resource in the Barents Sea. The Pacific oyster Crassostrea gigas was deliberately introduced to Europe in

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Bay barnacle Balanus improvisus. Image courtesy of J. Kotta.

Red macroalgae Asparagopsis armata. Image courtesy of M. Cormaci.

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1960. Although Pacific oysters directly introduced from the wild have been source of several cryptic diseases, and uncontrolled harvests of oysters contaminated by microbiota can lead to diseases of humans, this species is now responsible for the main biomass of mollusc production in Europe.

BENEFITS • Stock enhancement; • Provide organic material, nutrients and

food; • Increase in biodiversity; • Increase of bioturbation and oxygen

availability (including oxygen production); • Better conditions for denitrification (shunt

for eutrophication); • Increase in water transparency; • Storage of nutrients; • Shelter or settling substrate for several

native species; • Protection of shoreline against erosion and

flooding; • Decreased numbers of previous

introductions; • Scientific and educational information; • Improved fishery harvest of wild catches or

aquaculture; • Management of coastal areas; • Bioremediation and biofilters; • Increased employment.

ACHIEVEMENTS AND GAPS Two examples of application of new methodologies: Traditional taxonomic analysis and approaches have proven non-satisfactory not only in assesseing biodiversity, but also in taxonomic identification of alien species and studies of their likely area of origin. Molecular tools offer rapid and accurate means to obtain reliable infromation in these aspects. There are several recent examples on how these approaches have been applied. For instance, nucleotide sequence analysis of ribosomal RNA (rRNA) was used for taxonomic identification of ctenophores collected in the northern Baltic Sea, where alien Mnemiopsis leidyi and the native Pleurobrachia pileus have been reported to occur. The genetic analysis showed that, contrary to previous reports, there was only one specie called Mertensia ovum, a ctenophore with a broad Arctic and circumboreal distribution, which has never been reported to occur in the Baltic Sea.

Through simulations of a coupled model of bioenergetic-based anchovy population dynamics and lower trophic food web structure it became evident only recently how interaction of different factors resulted in the unprecedented 1989–90 anchovy–Mnemiopsis shift in the Black Sea. It appeared that combination of the density dependent effects of overfishing, eutrophication-induced nutrient enrichment, climate-induced over-enrichment and temperature-controlled Mnemiopsis spring production were jointly involved in the shift. Knowledge gap: The assessment of genetic impacts of alien species on native organisms is a relatively new field of research. It has been possible since relatively recently to detect genetic changes at the level of single genes. Therefore, perhaps the most understudied impact of alien species may be the genetic impacts they have on native biota. Today, the knowledge on changes in the genetic integrity of indigenous populations resulting from alien species introductions and genetically-modified organisms is mainly limited to hybridization events.

INTERNATIONAL COOPERATION Conventions, organisations and regulations: The United Nations Convention on the Law of the Sea (UNCLOS) explicitly places a general requirement for parties to take measures “to prevent, reduce and control pollution of the marine environment resulting from…the intentional or accidental introduction of species alien or new, to a particular part of the marine environment, which may cause significant and harmful changes thereto” (Article 196). The Convention on Biological Diversity (CBD) sets commitments for maintaining the world’s biological diversity with three main goals: conservation of biological diversity, sustainable use of its components, and fair and equitable sharing of the benefits from the use of genetic resources. Article 8h of the Convention calls on parties to prevent the introduction of, control, or eradicate those alien species that threaten ecosystems, habitats or species. The Global Invasive Species Programme (GISP) is an international partnership with the aim of conserving biodiversity and sustaining livelihoods by minimising the spread and impact of invasive species. It provides support

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Zebra mussel Dreissena polymorpha. Image courtesy of J. Kotta.

Zebra mussel Dreissena polymorpha. Image courtesy of J. Kotta.

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to the implementation of Article 8(h) of the CBD (http://www.gisp.org). International Convention on the Control and Management of Ships’ Ballast Water and Sediments (BWMC): The main goal of the of the International Maritime Organisation (IMO) is to prevent, minimize and ultimately eliminate the transfer of harmful aquatic organisms and pathogens through the control and management of ships' ballast water and sediments.

The EC "Regulation for use of alien and locally absent species in aquaculture" (EC, 2007) establishes a system for assessment and management of the risks associated with the introduction of new organisms for aquaculture.

Helsinki Convention (HELCOM): As a part of the HELCOM Baltic Sea Action Plan (BSAP), the road map towards ratification and harmonized implementation of the BMWC was adopted in 2007. According to BSAP, HELCOM countries agreed to ratify the BWM Convention as soon as possible, but by 2013 at the latest.

Oslo-Paris Convention (OSPAR): The Quality Status Report 2010 will provide an up-to-date evaluation of the marine environment of the North-East Atlantic, summarising ten years of assessment work under the OSPAR. Nonindigenous species are identified as a relevant pressure of human activities in the OSPAR Maritime Area.

Barcelona Convention: Nonindigenous species and their impacts are considered in the context of protected areas. The protocol concerning the Mediterranean Sea as a specially protected area obliges Parties to take measures in order to protect these areas. The measures may include the prohibition of the introduction of exotic species and the regulation of the species introductions in protected areas.

The International Council for the Exploration of the Sea (ICES) noted the risks associated with uncontrolled species introductions and transfers almost 40 years ago. Today ICES has two working groups to address the issue, i.e. the ICES Working Group on Introductions and Transfers of Marine Organisms (WGITMO) to deal with the movement of NIS for e.g. aquaculture purposes and the ICES/IOC/IMO Working Group on Ballast and Other Ship Vectors which focuses on species movements with ships.

ICES Code of Practice on the Introduction and Transfers of Marine Organisms. It follows the precautionary approach adopted from the FAO principles, with the goal to reduce the spread of exotic species. It accommodates the risks associated with current commercial practices including trade of ornamental species and bait organisms, research, and the import of live species for immediate human consumption. It also includes species that are intentionally imported to eradicate previously introduced invasive species, as well as genetically modified organisms and polyploids. It outlines a consistent, transparent process for the evaluation of a proposed new introduction.

RESEARCH FRAMEWORKS Several aspects of biological invasions were considered in a number of recently completed EU framework projects. These are:

DAISIE: Inventory of all known alien species in Europe and identification of the top 100 ‘worst’ invaders, their distribution and spread. This project summarised the ecological, economic and health risks and impacts of the most significant species (http://www.europe-aliens.org/).

ALARM: Management of alien species with the development of toolkits and recommendations in terms of environmental policy, the interaction of invasive alien species and sociology, climate change and chemicals. One of the project’s products was the development of the biopollution assessment system (http://corpi.ku.lt/~biopollution/).

IMPASSE: Development of guidelines and policies for environmentally sound practices for introductions and translocations in aquaculture that also covers quarantine procedures as well as risk assessments and assesses the impacts of invasive alien biota in aquaculture, protocols and procedures for assessing the potential impacts of invasive alien species in aquaculture and their economic impact (http://www.hull.ac.uk/hifi/IMPASSE).

MARBEF: Network of excellence, consisting of almost 100 European marine institutes, a platform to integrate and disseminate knowledge and expertise on marine biodiversity, with links to researchers, industry, stakeholders and the general public (www.marbef.org).

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Finding new life.

Legacies

Some of the legacies that the Census and European Census of Marine Life hope will endure post 2010 are:

• A sustained and dynamic EurOBIS and OBIS that serves the needs of the scientific community, as well as those of governments, industry, and educators;

• Technology and approaches that have been tried and tested in terms of surveying biodiversity in the oceans, that can be replicated globally by researchers as well as implemented within coastal and ocean observation systems and within monitoring programmes;

• An increased interest by the public in the oceans, the fauna that live there ultimately continued support for ongoing research,

• The development of marine biodiversity centres of excellence which will help build capacity in developing nations, and finally

• The identification of a new generation of ocean biogeographers and marine ecologists.

We hope that as you read this brochure, you discover some of the amazing things that have been discovered by Census researchers within Europe and that it increases your interest to find out more about the world’s oceans.

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References

Aquatic Invasions: International Journal of Applied Research on Biological Invasions in Aquatic Ecosystems. http://www.aquaticinvasions.net Bakran-Petricioli, T., Vacelet, J., Zibrowius, H., Petricioli, D., Chevaldonné, P., Rađa, T. 2007 New data on the distribution of the 'deep-sea' sponges Asbestopluma hypogea and Oopsacas minuta in the Mediterranean Sea. Marine Ecology 28: 10-23. Biological Invasions: http://www.springer.com/life+sciences/ecology/journal/10530 Bouchet, P. 2006 The magnitude of marine biodiversity. In: Duarte, C. M. (Ed.) The Exploration of Marine Biodiversity. Scientific and Technical Challenges. Fundación BBVA, Bilbao. 33-62. Bray, R. 2004 Steringovermes notacanthi n. g., n. sp. (Digenea: Fellodistomidae) from the deep-sea spiny eel Notacanthus bonaparte Risso (Notacanthiformes: Notacanthidae) from the NE Atlantic and a new host record for Olssonium turneri. Bray and Gibson, 1980. Zootaxa 684: 1-7. Carcupinio, M., Floris, A., Addis, A., Castelli, A., Curini-Galletti, M. 2006 A new species of the genus Lightiella: the first record of Cephalocarida (Crustacea) in Europe. Zoological Journal of the Linnean Society 148: 209–220. Chenuil, A., Egea, E, Rocher, C., Touzet, H., Feral, J-P. 2008 Does hybridization increase evolutionary rate? Data from the 28S-rDNA D8 domain in echinoderms. Journal of Molecular Evolution 67: 539-550. Coll M., Piroddi C., Steenbeek J., Kaschner K., Ben Rais Lasram F., et al. 2010 The biodiversity of the Mediterranean Sea: Estimates, Patterns and Threats. PLoS ONE 5(8): e11842; doi:10.1371/journal.pone.0011842 Costello M.J., Coll M., Danovaro R., Halpin P., Ojaveer H., et al. 2010 A Census of Marine Biodiversity Knowledge, Resources, and Future Challenges. PLoS ONE 5(8): e12110. doi:10.1371/journal.pone.0012110 Costello, M.J., Emblow, C., White, R. 2001 European Register of Marine Species. A check-list of the marine species in Europe and a bibliography of guides to their identification. Patrimoines Naturels 50: 463pp. DAISIE. 2009 Handbook of alien species in Europe. Springer, Dordrecht. Danovaro R., Company J.B., Corinaldesi C., D’Onghia G., Galil B. et al. 2010 Deep-Sea Biodiversity in the Mediterranean Sea: The known, the unknown and the unknowable. PLoS ONE 5(8): e11832; doi:10.1371/journal.pone.0011832 EEA 2006 Priority issues in the Mediterranean Sea. European Environment Agency Report El-Rashidy, H.H., Boxshall, G.A. 2009 Parasites gained: alien parasites switching to native hosts. Journal of Parasitology 95: 1326-1329. Galil, B. S. 2008 Alien species in the Mediterranean Sea. Which, when, where, why? Hydrobiologia 606: 105–116. Golani, D., Orsi-Relini, L., Massuti, E., Quignard, J.-P. 2002 Fishes. In CIESM Atlas of exotic species in the Mediterranean (ed. F. Briand). CIESM Publishers, Monaco, 256 p. Gollasch, S. and Leppäkoski, E. 1999 Initial risk assessment of alien species in Nordic coastal waters. Nordic Council of Ministers, Copenhagen.

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