Diversity of European Seas Finding New Life

The European Census of Marine Life Diversity of European Seas - Finding New Life

Fi nding new life.

Authors Acknowledgements Bhavani E Narayanaswamy The European Census of Marine Life was Scottish Association for Marine Science, funded by a number of different sources. In Scottish Marine Institute, Oban, Argyll, UK particular we would like to acknowledge the support given to us by Foundation TOTAL, Henn Ojaveer the Alfred P Sloan Foundation, the Stavros Estonian Marine Institute, University of Tartu, Niarchos Foundation and Argyll and Islands Parnu, Estonia Enterprise. In addition much of this work would not have been able to be undertaken Geoff Boxshall had it not been for the research undertaken Department of Zoology, The Natural History by the numerous scientists working in Museum, Cromwell Road, London, UK European Waters, the support given by the different European marine science Ward Appeltans Institutions and Universities, as well as the Flanders Marine Institute, Wandelaarkaai 7, funding agencies in each country. Oostende, Belgium For all correspondence relating to this report Roberto Danovaro please contact [email protected] Polytechnic University of Marche, Via Brecce Bianche, Ancona, Italy For more information, please visit www.eurocoml.org Poul Holm Trinity Long Room Hub, Trinity College Images courtesy of J Stafford-Deitsch, R Dublin, Ireland Hopcroft, B Bluhm, K Iken, H Brown, D Fiege, K Rascoff. Thom Nickell Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, UK

Editors Citation Bhavani E Narayanaswamy, Olga Kimmins Narayanaswamy, BE, Ojaveer H, Boxshall and Henn Ojaveer. G, Appeltans W, Danovaro R, Holm P and Nickell T. (2010) Diversity of European Seas - Finding New Life. EuroCoML Non- Technical Report, Oban, UK.

Fi nding new life. Contents: Contents:Preface 5 Preface 5 Introduction 8 Introduction 8 History of Marine Animal Populations 14 History of Marine Animal Populations 14 Species Abundance, Diversity, Distribution 20 Species Abundance, Diversity, Distribution 20 Zooming in on the detail 24 Zooming in on the detail 24 Biodiversity in European Seas 37 Biodiversity in European Seas 37 Alien species 44 Alien species 44 Legacies 53 Legacies 53 References 54 References 54

ife. Finding new l F i nding n ew li fe.

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 Contents: of the nearly 3,000 researchers involved from more than 80 nations. Contents:Preface 5 Preface 5 Alongside the Census field projects, and the projects exploring the Introduction 8 history and trying to make predictions for the future, have been the 13 Introduction 8 National and Regional Implementation Committees (NRICs), of which Europe is one. One of History of Marine Animal Populations 14 the NRICs main roles has been to promote the Census to researchers, the public and other History of Marine Animal Populations 14 stakeholders within their countries and regions. This was just one of Europe’s main aims. Species Abundance, Diversity, Distribution 20 Europe has been extremely successful in working with the projects already running within the Species Abundance, Diversity, Distribution 20 Census framework as well as highlighting areas of research that are of particular importance Zooming in on the detail 24 to Europe, for example the impact of invasive alien species. Through collaborative research, it Zooming in on the detail 24 has been found that there are likely to be more than 1,200 alien species in European waters Biodiversity in European Seas 37 alone, several hundred more than were previously thought. Other work highlighted by Biodiversity in European Seas 37 researchers in Europe has been the changes in fish communities in European waters over Alien species 44 numerous centuries. Some of this information is being used to help forecast what fish species Alien species 44 may inhabit European waters as air and sea temperatures rise. At the start of the Census Legacies 53 ~29,000 marine species were known in European waters and as the “Decade of Discovery” Legacies 53 peaks, we now estimate that there are almost 32,000 species living in European seas! These References 54 discoveries have also highlighted where there are gaps in our knowledge; in European waters References 54 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 countries. 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.

F life. inding new . Fin F i nding n ew li fe ding new life.

Contents: Contents:Public perception and appreciation of the oceans is growing, even without the events in the PrefaceGulf of Mexico this yea r. The incredible value brought by a programme, such as the Census 5 of Preface 5 Marine Life, which eschews normal “hypothesis-driven” research favoured by funding Introductionagencies in contrast to invigorating the spirit of discover y, has truly forged a bond between 8 Introduction 8 European marine scientists and our colleagues around the world. I was fortunate to have the

Historyopportunity of Marine to chair Animal the PopulationsEuroCoML for over five years and to see the programme and14 its History of Marine Animal Populations 14 discoveries grow year by year. This would not have been possible without the dedication of the programmeSpecies Abundance, manager ,Diversit Bhavaniy, DistributionNarayanaswam y, and the whole steering committee. I would20 Species Abundance, Diversity, Distribution 20 also like to pay tribute and honour the late Professor Alasdair McIntyre for his vision and guidance,Zooming in and on themy detailsuccessor Henn Ojaveer and his co-chair Isabel Sousa-Pinto, for steering24 Zooming in on the detail 24 us all to a successful conclusion that truly marks a Decade of Discovery. Biodiversity in European Seas 37 Biodiversity in European Seas 37 ProfessorAlien species Graham Shimmield, 44 Alien species 44 Former Chair, European Census of Marine Life BigelowLegacies Laboratory for Ocean Sciences 53 Legacies 53 References 54 References 54

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Historyopportunity of Marine to chair Animal the PopulationsEuroCoML for over five years and to see the programme and14 its History of Marine Animal Populations 14 discoveries grow year by year. This would not have been possible without the dedication of the programmeSpecies Abundance, manager ,Diversit Bhavaniy, DistributionNarayanaswam y, and the whole steering committee. I would20 Species Abundance, Diversity, Distribution 20 also like to pay tribute and honour the late Professor Alasdair McIntyre for his vision and Hermit crab walking on a seastar in UK waters. Image courtesy of H. Brown. guidance,Zooming in and on themy detailsuccessor Henn Ojaveer and his co-chair Isabel Sousa-Pinto, for steering24 Zooming in on the detail 24 us all to a successful conclusion that truly marks a Decade of Discovery. Biodiversity in European Seas 37 Biodiversity in European Seas 37 ProfessorAlien species Graham Shimmield, 44 Alien species 44 Former Chair, European Census of Marine Life BigelowLegacies Laboratory for Ocean Sciences 53 Legacies 53 References 54 References 54

Mako shark. Image courtesy of J Stafford-Deitsch.

ife. Finding new l F i nding n ew li fe. 7 8 Introduction

WHAT IS THE CENSUS OF MARINE become more aware of the lack of data in LIFE? certain areas and depths of the oceans.

The Census of Marine Life is a growing global With regards to diversity there are numerous network of researchers from more than 80 lists and collections of specimens residing in nations that have been involved in a ten-year natural history museums, laboratories and (2000-2010) scientific initiative. 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 WHY THE NEED FOR A CENSUS OF that by the end of 2010 most of the old species MARINE LIFE? records and all of the new ones will have been entered into the database. Not only is it hoped About 70% of the Earth’s surface is covered by for all the data to be in OBIS but for every ocean and of this it is estimated that only 5% species to have an entry in the Encyclopaedia of the ocean has been explored. By of Life (www.eol.org), whereby pictures, comparison to the land, relatively little is known references and general information for every about the animals living in the world’s oceans, species, both marine and terrestrial, can be and even less about those that inhabit the found. depths of the ocean; more than half the ocean is deeper than 3,000 metres. Much of the Species diversity does not always remain research that has previously been undertaken static with changes in diversity attributed to has concentrated mainly on the more many different factors including changes in the accessible near-shore regions and down to a world’s climate as well as fishing. Hot spots of depth of about 1,000 metres. diversity occur in the oceans just like they occur on land, particularly for the larger To increase our knowledge and understanding animals such as fish. By finding out more of the life that inhabits the world’s oceans, the information about these hotspots it is hoped Census of Marine Life was formed. The that these larger animals may be protected. overarching aim of the Census is to both assess and explain the diversity, distribution The distribution of species has become even and abundance of life in the oceans. Within more important as old records have been this framework the Census proposed what investigated. Of particular interest is the appears to be three very simple and change in species range and territory and straightforward questions and upon which the trying to find the reasons as to why this is foundations of the Census has been built. occurring; is it due to changes in climate? They were: Abundance was the third aspect of importance • What did live in the oceans? to the Census. Researchers were not only • What does live in the oceans? interested in the diversity and distribution of • What will live in the oceans? the fauna, but also in trying to determine how many individuals of each species there were in Prior to the Census of Marine Life, the lists of different regions. In the marine science species held by different institutions around the community, both actual numbers of a species world was accessible to a limited number of and also its weight (biomass) are of interest. people. Through the Census, the Ocean Biogeographic Information System (OBIS; 14 field programmes were instigated by the http://www.iobis.org) was formed and scientists Census of Marine Life; many of those either and researchers with access to species lists have a scientific project running within Europe, were asked to add/send data to OBIS. Europe or have European researchers involved (see also has its own OBIS called EurOBIS text box). The projects cover: (http://www.marbef.org/data/eurobis.php) • The whole size spectrum of maintained by the Flanders Marine Institute. It organisms, ranging from microbes to is through this that scientists, non-government whales; organisations and other stakeholders have

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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.

8 9 10 • The vast depth range from the shore • Increase European participation in line to the deep-sea; several particular CoML projects • The tropics to the poles; where untapped potential remains; • A number of different habitats from • Improve marine taxonomy and species underwater mountains (seamounts) to data in the European region; the vast expanse of the abyssal plains; • Improve biodiversity and ecosystem • Employ a variety of technology ranging information for applied resource from placing tags that capture management in waters where environmental and biological data on European nations hold major individual animals to cameras that influence; film/take still images of animals in their • Improve awareness of the Census with home environment to genetic the wider public. techniques that can be used on larvae/animal fragments to help with EuroCoML was successful in the aims listed their identification. above, particularly in making links with programmes already funded and running in Europe. These included the EU Network of WHY THE NEED FOR A EUROPEAN Excellence – Marine Biodiversity and CENSUS OF MARINE LIFE? Ecosystem Functioning (www.marbef.org), the EU FP6 programme Hotspot Research on the The European Census of Marine Life Margins of European Seas (www.eu- (EuroCoML) is a Regional Implementation hermes.net) and its daughter programme Committee for the Census. National and Hotspot Ecosystem Research and Man’s Regional Implementation Committees (NRICs) Impact on European Seas (www.eu- were formed to assess the known, unknown hermione.net), to name but a few. and unknowable about marine biodiversity in local waters. In addition it was anticipated that EuroCoML was also very active in promoting the NRICs would be able to ensure that the the results from the Census and engaging with aims, results and outcomes of the Census the public by giving talks, producing posters, reached as wide an audience as possible, flyers and newsletters to a wide range of including scientists, non-government audience types (www.eurocoml.org). organisations and the general public amongst others. EuroCoML is one of 13 NRI As the first Census draws to a close at the end committees that were formed with the remit to of 2010 it is hoped that the data that have support, promote and synthesise results that been gathered and the results that have been address the environmental and societal needs synthesised will: of communities within their region of operation. • Advance the knowledge of life in the As can be seen from the map (p.14), world’s ocean; EuroCoML covers one of the largest areas of • Produce a catalogue of marine all the NRICs; from Greenland in the west to species; Vladivostok in the east and from the • Help provide information so that Mediterranean Sea in the south to the Arctic in decisions relating to managing marine the north (includes the Arctic, North Sea, Baltic resources can be carefully undertaken. 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;

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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.

12 13 13 Fig. 1. NRIC Regions and Sub-Regions. Image courtesy of M. Costello

Arctic Sea

Baltic North Sea Sea

NE Atlantic Ocean

Mediterranean

Fig. 2. Marine Research Institutes in Europe. Image courtesy of M. Coll

12 13 14 History of Marine Animal Populations

HOW MAY WE LEARN FROM INSIGHTS FROM MONASTIC HISTORY? RECORDS – THE WHITE AND BARENTS SEA To understand the interaction of humans and the oceans we need to bridge the divide On the shores of the White and Barents seas between history and science. Historical in northern Russia, Orthodox monks have kept research can provide baselines of ocean meticulous records of the landings from the abundance and species distribution in the past sea and rivers in the area since the 16th and inform us of the scale of human impact century. Atlantic salmon was one of the most through time. Historical research will inform us valuable products of the local economy, being of how much society depended on ocean extracted mostly in the lower parts of rivers, resources for economic, social and cultural using weirs that remained technologically needs. We need this knowledge not only to unchanged over the centuries. This makes understand our past but also to predict ocean fishing effort measurable over time and allows resilience in the future. comparison of historical catch data for the 17th and 18th centuries with the statistical data that The History of Marine Animal Populations are available from the end of the 19th century. (HMAP) project was constituted as four sub- The study based on historical catch data from groups for the seas around Europe: the North several locations showed that size of salmon Sea, the Baltic, the Mediterranean and the populations in the Russian North before the Black Sea, and the White and Barents Seas. mid-20th century depended mostly on climatic Thanks to the collaborative efforts we are now fluctuations, with salmon abundance in a position to begin to piece together a increasing in warmer periods. After about picture of human interaction with marine life in 1950, most populations declined due to the European seas in the past 500-2,000 overfishing, the development of timber years. industry, dams and pollution.

We now know enough to quantify the removals Signs of climate-related dynamics were by human exploitation of several commercial observed also on other fish, such as cod, target species. We have a good sense of the halibut and herring, although correlation did importance of human interaction for the not approach statistical significance. In nearshore ecosystems, are beginning to particular, the White Sea herring fishery, of understand the importance of marine products economic importance since the 18th century, for human consumption, and have a much showed considerable short-term fluctuations of better basis from which to assess the main catches due to both social and natural factors drivers of human marine exploitation. These and their interaction, which may confound insights are critical not only to our climate effects. Climate effects were also understanding of the past but also to st pronounced on Arctic marine mammals such management in the 21 century, when the as white whales, Greenlandic seals, narwhales oceans will be the last part of the biosphere to and others, which considerably changed their be exposed to a change from hunting to distribution patterns migrating to more cultivating practices. southern regions than usual in cold periods of 1800-1809 and 1877-1903, and again in 1970- The breakthrough is due to the introduction of 80. established marine science methodology to historical data, notably standardising fishing For marine mammals anthropogenic pressure effort (catch-per-unit effort), zoo-archaeological became a significant factor earlier than for fish. analysis of marine animal remains, biodiversity Hunting impacted the general dynamics of the counts of historical fisheries, statistical population of the eastern walrus from at least modelling of historical data, etc. 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

14 15 15 hunting techniques in the late 19th century certain weekdays and through the forty resulted in a considerable decrease of the weekdays of Lent. walrus population by the middle of the 20th century. For fish, particularly for Atlantic salmon, clear stress signals related to human AN ANCIENT FISHING INDUSTRY – activities such as overfishing and development THE MEDITERRANEAN AND BLACK of forestry with timber-rafting became apparent only by the end of the 19th century. SEAS

The Mediterranean and Black Sea are among the earliest heavily fished marine ecosystems INSIGHTS FROM FISH BONES in the world. Fish was an important source of food in the coastal and riverine cultures of the Some climate models predict that air and sea ancient Mediterranean. Until quite recently, temperatures will rise by approximately 3°C historians have assumed that the ancient during the next 70-100 years. In order to fisheries were of minimal importance, understand some of the processes by which technology was simple and nets were cast suggested global warming might affect marine from the shoreline. A full reversal of this fish species near Denmark, researchers have perception was only achieved as a result of an investigated the fish fauna during one of the analysis of the historical evidence matched by warmest prehistoric periods, the warm Atlantic an understanding of modern impact studies of period (around 7000-3900 BC). A total of pre-industrial fisheries technology. The ancient 108,000 fish bones were identified, and Greeks and Romans went to sea to fish with amongst them were bones of many species, hook-and-line as well as nets. Ancient for example anchovy and black sea bream, technology was neither ineffective nor which we usually consider to be typical of unproductive, and indeed produced such large waters much farther south and warmer, like the catches that transport, preservation and Mediterranean Sea. When temperatures storage became the limiting factors. One cooled after the warm period ended, most of solution to the problem of conserving the fish these species disappeared from the was to dry and salt it. The most spectacular archaeological record, suggesting that local solution, however, was the reduction of fish to abundances declined. However, many of those fish sauce – garum – essentially by fermenting same warm-water species have recently the catch in large vats to produce a liquid reappeared in waters around Denmark as which was traded all over the Roman world to temperatures have risen in the last 10-15 add flavour to the Roman cuisine. The largest years. The archaeological information can be production installations were located near the an indicator of which species may become Straits of Gibraltar and on the northern shore common as climate changes and warms. of the Black Sea. The largest installation in present-day Mauretania had a capacity of over The period circa 950-1050 saw a major rise in 1,000 cubic metres of fish sauce. fish consumption around the North Sea. Early medieval sites are dominated by freshwater The fishing industries in the Mediterranean and and migratory species such as eel and salmon, Black Seas collapsed in the early medieval while later settlements reveal a widespread period and heavy fishing only commenced in consumption of marine species such as early modern times. The seas have been herring, cod, hake, saithe and ling. The “fish th heavily fished through the last few hundred event” of the 11 century reflected major years and ecosystems have been modified economic and technological changes in dramatically by human interventions. History coastal settlements and technologies and projects have reconstructed the dynamics of formed the basis of dietary preferences that th marine animal population in the Venetian were to last into the 17 century. The evidence Lagoon and in the Northern Adriatic Sea from also supports a hypothesis that sea-going th st th the 12 century up to the 21 century from vessels were in wide use by the 13 century, historical and scientific sources. A study of the catching deep-sea fishes such as ling which Catalan Sea showed that the impact of modern would require lines of several hundred metres. trawling in the 20th century was particularly Commercial fisheries were well established by severe. Large parts of the Mediterranean and the High Middle Ages and would feed a Black Seas are heavily fished down and we European population which by the same time are only now beginning to realise the had developed religious practices of fasting immensity of change and loss. and abstinence of red meat in favour of fish at

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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.

16 17 17 20TH CENTURY – THE BALTIC SEA Swedish and Scottish participation. By 1870 total removals reached a level of 300,000 One of the early research questions posed by tonnes, which equals the recommended Total HMAP researchers concerned the eastern Allowable Catch for 2007 for herring in the Baltic cod population. In the absence of North Sea (ICES 2006). This evidence historical records for the period before 1966, demonstrates how fishermen in the age before they wondered if the record high cod stock in steam and trawl were able to remove large the Baltic Sea in the late 1970s and early quantities of biomass from the sea. The 1980s was a unique occurrence or likely to technologies of wind power and driftnets were practically unchanged in the Dutch fisheries occur at regular intervals. The question was th th th unequivocally answered by the work of the from the 16 to the 19 centuries. In the 20 Baltic team. Through the recovery of historical century total catches repeatedly amounted to data going back to 1925, we now know that well over a million tonnes annually, causing abundant cod stock corresponded to a collapses of herring stocks and the closure of favourable combination of four key drivers in fisheries for one or two decades to allow the late 1970s: incursions of saline water to the populations to rebuild. brackish Baltic and hydrographic conditions allowing successful reproduction of cod; low marine mammal predation; high productivity COD AND HADDOCK environment fuelled by nutrient loading; and reduced fishing pressure. A similar situation Catches of cod and haddock were abundant in did not occur at any other time in the 20th the second half of the 19th century while the century. The cod biomass in the 1920s-1940s stocks showed signs of depletion by the First was likely restricted by high abundance of World War. Detailed historical data are marine mammals and low ecosystem available from the Swedish fishery in the north- productivity, and in the 1950s-1960s by high eastern North Sea and Skagerrak, which make fishing pressure. Deteriorating hydrographic up about one sixth of the entire North Sea. conditions have been pronounced since the From these data the minimum total biomass of late 1980s, thereby restricting cod recruitment. cod in 1872 has been estimated at about Today, cod rarely ventures into the northern 47,000 tonnes for this portion of the North Sea, Baltic waters between Stockholm (Sweden) but it may have been much higher, while the and Saaremaa Island (Estonia). During much total biomass of ling was estimated at a total of earlier times, in the late 16th and the early 17th 48,000 tonnes. These were very healthy centuries, the presence of a large cod fishery stocks if the levels are compared with the off southern Finland indicates that cod must modern biomass estimate for cod of 46,000 have been abundant in the northern Baltic. The tonnes for the entire North Sea, Skagerrak and abundance is all the more remarkable because Eastern Channel. For ling no biomass estimate the population of top predators, such as seals, is available as the species is caught too would have been much larger than it is today, infrequently. with the ecosystem being oligotrophic.

EXTIRPATIONS IN THE NORTH SEA WHEN A SPECIES DECLINES AND RECOVERS – THE NORTH SEA Few marine animals have gone extinct in the last few thousand years when human hunting The first evidence of total removals from the and fisheries may have contributed to species North and Baltic Seas comes from the Danish depletion. The fact that few marine species inshore fisheries in Scania and Bohuslen for have gone completely extinct is no doubt herring in the 16th century. By then annual related to the fact that human activities on the catches regularly reached a level of 35,000 global scale have been restricted to nearshore th and midwater realms until the last half of the tonnes. By the late 16 century, the Dutch had th taken the lead in Northern European herring 20 century. However, human activities, fisheries with sea-going buysen which including extraction and disturbance, have harvested the rich schools off the coasts of spanned the entire North Sea since at least Scottish mainland and the Orkneys. Total about 800 AD when Vikings were noted to catches with English, Scottish and Norwegian have made a direct crossing of the North Sea landings amounted to upwards of 100,000 from Scandinavia to Northumbria, “something tonnes. Catches declined to about half of that never thought possible before,” according to level by 1700, and only increased to about Bishop Alcuin. 200,000 tonnes in the late 18th century due to

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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.

18 19 19 Pelicans disappeared from the Wadden Sea 1770s was on the increase again. We have region of the southern North Sea about 2,000 evidence of an abundant haddock fishery by years ago but the cause of their disappearance German and Danish hand liners in the German is not known. The Atlantic Gray Whale went Bight and up along the Jutland coast in the late extinct not only from the North Sea but as a 18th century and first half of the 19th. Statistics species sometime in the late medieval period, show substantial catches by 1875, which and we may suspect human hunting and declined rapidly in the last quarter of the disturbance practices to have contributed to century to nil around 1910. It would seem that the decline of the species, but we have no the southern North Sea haddock stocks were direct evidence to substantiate the claim. The rendered commercially extinct by the intensive disappearance of the Great Auk, on the other German and Fanø-Hjerting fisheries of the late hand, was certainly caused by widespread 19th century. Today, haddock is prevalent slaughter of the flightless bird on the coasts of mainly in the northernmost part of the North the North Sea and North Atlantic. The bird Sea and in the Skagerrak, while its former disappeared from the North Sea in the Late widespread presence in the southern part of Middle Ages and the last birds were killed on the North Sea was not recognized by marine St Kilda in 1840, in Iceland in 1844 and in science until recently. South West Greenland the same year.

While species extinction is rare in the marine PUBLICATIONS realm, a number of species have been so much reduced in numbers that they are HMAP research has been published in more considered regionally extinct or at least so rare than 200 books and papers. Publications can that they have lost their ecosystem be accessed through several databases: importance, and their previous commercial importance to the human economy. • For identifying publications concerning a specific marine area visit the HMAP Regional extinctions have occurred mainly in th th website and look at the dedicated the late 19 and 20 centuries. Sturgeon was project webpage. Here, all the previously caught in vast quantities and publications regarding the area are marketed in their hundreds at the Hamburg listed along with the contact fish auction, for instance. By 1900, however, information for the project leader. the fishing declined rapidly both due to river www.hmapcoml.org and inshore pollution and to fisheries. As late as the 1930s sturgeon was still caught • At the CoML Bibliographic Database, regularly in the northern Danish part of the all the HMAP publications are listed Wadden Sea but is now extremely rare. While and searchable by all criteria. the sturgeon was easily caught by nets, the http://db.coml.org/comlrefbase blue-fin tuna escaped human hunting activity th until the 20 century due to its rapidity and • HMAP Data Pages. By the end of superior strength which made the catch 2010 the data pages will contain more impossible. By the 1920s superior hook-and- than 1,000,000 data extracted from the line technology was available and brought tuna HMAP project. The data are online within the reach of fishermen. Even more and freely accessible. The HMAP Data importantly, harpoon rifles were deployed in Pages are a research resource. the 1930s and rapidly increased catches to www.hull.ac.uk/hmap thousands of individuals per year. By 1950, however, tuna catches dropped, and ceased to • Historical Atlas of Marine Ecosystems be of commercial importance after 1955. HMAP has developed a dynamic, Climate change and prey abundance seem online historical atlas of marine unlikely causes for the sudden decline, and it ecosystems. Using Google Earth and now seems possible that the commercial Open Layers, HMAP collects extinction of blue-fin tuna from the North Sea information from historians, ecologists, was caused by the heavy onslaught by th archaeologists and fishermen to map humans in the mid-20 century. how marine life and ecosystems in the oceans have changed over time. In the southern North Sea, the haddock fishery http://hmap.unh.edu. was of substantial size in the 16th and first half th of the 17 centuries. The fishery declined in Website: www.hmapcoml.org the later 17th into the 18th century but by the

18 19 20 Species Abundance, Diversity, Distribution

CHALLENGES TO STUDYING LATITUDINAL SPECIES DIVERSITY MARINE DIVERSITY GRADIENTS

One of the historic challenges in marine The data sets examined from the Northeast biology has been to understand why marine Atlantic contain around 10,000 species, which organisms live where they do. Anyone who allows scientists to test their hypotheses on has been to the seaside has probably noticed diversity. For questions related to definable that different areas of the sea have different geographical areas of the ocean, some groups characteristics – here a shallow sandy bottom, such as polychaete worms are more useful there a muddy, silty plain. Of course, in the than others, as they can be found across all of Northeast Atlantic there is a myriad of different the areas, perform a number of different environments where life flourishes, and the ecological functions, and have a variety of physical characteristics are not just different feeding types and lifestyles. One constrained to the sediment type (sandy or question is known as the Latitudinal Species muddy), but include among many others Diversity Gradient (LSDG): this postulates that depth, temperature, food availability and there should be a decrease in the number of latitude. species with increasing latitude. Using the Macroben data base, no such northward decrease in diversity could be found in the CRADLE OF EUROPEAN DEEP deep sea, once factors such as depth and WATER RESEARCH sampling effort were accounted for. This finding is surprising, as intuitively one might

The Northeast Atlantic has been seen as the expect the more northerly European seas to cradle of deep sea research, due to its resemble more closely the relatively species- accessibility to the early marine research poor Arctic Ocean. The highest species laboratories established in the 19th century. diversity occurs in the Norwegian and Barents Many of these laboratories and learned Seas, possibly because of the influence of societies established surveys of the bottom- warm water currents from the Gulf Stream living (benthic) animals by sampling along system bringing water and organisms from the depth gradients, often beginning in the shallow North Atlantic. coastal margins and continuing down the continental slope to the abyssal plains below. On a regional scale, the North Sea would Recent projects such as MarBEF, Census and appear to show an actual increase in diversity EuroCoML have analysed very large data sets with increase in latitude; the shallow, sandy, of benthic animals to attempt to answer some heavily trawled southern North Sea is fairly fundamental questions on the distribution markedly less diverse than the deeper, siltier, of marine animals, such as: does biodiversity less intensively fished northern part. There are, increase or decrease in benthic animals with however, so many physical differences increasing latitude; does diversity decrease or between the southern and northern North Sea increase with depth; and what are the other that saying the difference in diversity may be important factors controlling benthic caused by the change in latitude is almost distribution and abundance across this huge irrelevant: there appear to be so many other area. At the heart of these seemingly simple factors at play in determining why diversity is questions, however, lie some basic greater in different areas of the North Sea. disagreements among scientists on how to actually measure diversity. For simplicity’s While there may be no noticeable LSDG in the sake, diversity can be thought of as the deep Northeast Atlantic among polychaete number of species present; when comparing worms, some taxonomic groups such as samples from different surveys taken with foraminiferans and molluscs have shown such different gear, a more complex index such as a gradient. Other groups such as nematode Hurlbert’s Rarefaction can be used, which worms indicate greater species richness with predicts how many species will be present for increasing latitude. What is clear from these a given number of individual animals in a particular studies is that different physical sample. 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.

20 21 22 certain groups of animals live. Also, scientific excess of 4,000 metres. Generally speaking, in surveys of these remote environments over the the eastern and western basins of the years have not used a standardised method of Mediterranean, diversity decreases with depth collecting samples, using different sized sieve among most animal groups apart from the meshes to separate animals from sediment, as single celled microorganisms (Archaea and well as using various coring and grabbing bacteria). While there are a high number of devices with different sampling efficiencies, as endemic species in the Mediterranean (around well as sampling across a wide range of 27%), most of these occur in the shallow habitats. All of these factors contribute to the coastal margins; the deep Mediterranean is lack of definitive answers to questions of relatively poorly studied and abundances here diversity gradients and latitude. are very low.

In contrast, the Baltic is a shallow, brackish CHANGES IN FAUNAL sea. With an average depth of 60 metres, the DISTRIBUTION Baltic only reaches 460 metres at its deepest. While there are roughly 6,000 species in total

In the early days of marine science it was inhabiting the Baltic, fewer than 1,500 of these thought that because fewer and fewer animals are benthic macrofauna. The main factors were collected the deeper one sampled, there influencing the distribution of marine life in the was a depth at which all life ceased to exist. Baltic are temperature, salinity and oxygen Although we now know this is not the case, depletion; the Baltic is strongly stratified, with many studies have noted that diversity does only periodic inflow of sea water from the change with depth. It is probably not increasing western entrance (the Kattegat), and ice cover pressure that is the cause of depth extends in the shallower areas from November distributions (pressure increases with depth), until mid-May. but more likely factors related to temperature, both absolute and range, that are affecting animal distributions. Using the North Sea data FACTORS INFLUENCING set mentioned above, a relationship was found DISTRIBUTION AND DIVERSITY between diversity and depth – the greater the depth, the more species present. In the case of As we have seen, there are a number of the North Sea, this might be due to the greater natural physical factors influencing the temperature range experienced in the southern distribution and diversity of marine life in North Sea, which could be preventing more European seas. In addition to these factors, northern species from surviving the higher man-made or anthropogenic pressures have summer water temperatures. also played a role; industrial activity, excessive nutrient input and fishing (especially bottom Away from the relatively shallow North Sea, trawling) have all had large impacts on marine the Northeast Atlantic continental slope life. For example, parts of the southern North regions generally show an increase in diversity Sea are fished 5-10 times per year; some down to 200 metre depth. Below that depth, species such as the common skate have been the number of species present generally fished to extinction in parts of their former declines to a depth of around 500 metres. In range. In the future we will see greater impacts the deep Northeast Atlantic it is generally from pollution and eutrophication as well as assumed that diversity of large (macrofaunal) from changes in the climate. All of these animals increases until some intermediate factors together will no doubt have a major depth, and then gradually decreases again influence on the diversity, distribution and without ever reaching zero; this relationship is abundance of life in the oceans. 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

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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).

22 23 24 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 as cold seeps, hydrothermal vents, cold water biome of the biosphere but, due to their corals, canyons and nodule areas. This has remoteness are extremely difficult to explore. resulted in an unprecedented direct sampling of these different habitats, which, was often not It is known that shallow water ecosystems are possible using traditional remote coring characterized by an extremely structural techniques. Such studies have shown that they complexity and habitat heterogeneity. Deep are occupied by benthic communities that are diving is now allowing the direct study of the different from those living in surrounding areas upper portion of the twilight zone, which is of typical deep-sea floor. Recent studies have revealing a similar extraordinary diversity of revealed that, conversely to what was substrates and organisms. The deep-sea floor hypothesised, deep-sea ecosystems are not has long been considered to be a relatively homogeneous, and include a highly homogeneous environment on a large scale, heterogeneous mosaic of habitats. Continental comprising vast areas of soft surface margin ecosystems such as coral mounds, sediments. Environmental factors, such as canyons or cold seeps can be distinguished food input, hydrodynamics and sediment from the open slope by their imprints on a composition, were assumed to be the main topographic map or sonar imagery. These drivers of differences in benthic biodiversity habitats are fundamental for explaining the and community composition. Only in the last high biodiversity observed in the deep-sea 20 year has the advent of new, highly systems and to the production of fisheries, sophisticated technology allowed us to energy and mineral resources, as well as the investigate these systems in detail and to shed critical ecological service of carbon light on the dark portion of the biosphere. As a sequestration. The complexity of the life forms, result of increasing exploration by means of including ‘ecosystem engineers’ able to create bathymetric and visual mapping of habitats hard structures such as carbonate reefs, there is now a growing awareness of the true pinnacles, tunnels etc. along with the erosive extent of habitat heterogeneity and associated effect of bottom currents, sediment diagenesis biodiversity along continental margins and and tectonic activity create a multitude of abyssal plains. Knowledge of the biological habitats only recently recognized as entities communities associated with, in particular, that support distinct communities and life locally restricted habitats in the deep sea, is forms. The characterization of habitats within increasing and we now have an understanding these ecosystems requires sampling and/or of how several variables such as substrate visual observations. Patterns of species availability and type, biogeochemistry, nutrient distribution evaluated in the context of input, productivity, hydrological conditions and relatively monotonous slopes and abyssal catastrophic events shape patterns of diversity plains must now be re-evaluated in the light of on regional scale. this newly recognized habitat heterogeneity.

With greater accessibility of remotely operated vehicles (ROV), there has been increasing interest in some deep-sea environments, such

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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- becoming increasingly clear. The deep stress oxygen minimum zones and methane continental margins (extending from shelf seeps, to vast reefs of sponges and corals, the break down to continental rise) are complex linkages between habitat heterogeneous at multiple spatial and temporal heterogeneity and high biodiversity are 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.

26 27 27

habitat the to contributing types system eco Tangherlini. Michael By

heterogeneity and complexity. complexity. and heterogeneity

main the illustrating landscape deep-sea conceptual A

26 27 28 SLOPES preferential areas for the recruitment of megafaunal species. Canyons probably play Slopes are by far the most widespread system an important role in structuring the populations present along continental margins. The and life cycles of planktonic fauna, as well as steepness of the slope allows the distinction benthic megafauna fishery resources that are between progressive, intermediate, and abrupt associated with them. For example, canyons continental margins. Landslides can shape the are important habitats for fished species, such seafloor and mobilize huge volumes of as hake (Merluccius merluccius) and for the sediments. Slopes are ideal systems for rose shrimp Aristeus antennatus. Because of investigating benthic biodiversity patterns, as their characteristics, the biodiversity of faunal these systems typically show the decrease of assemblages can be markedly different from benthic abundance and biomass with that on the adjacent open slopes. 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.

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

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 The three pictures illustrate the sessile and with only linear canyons (e.g. the Catalonia mobile fauna on hard bottom of a flank of a margin), or no canyons at all (e.g. the North deep-sea canyon along the Portuguese margin. Balearic margin). They represent hot spots of Projects HERMES and HERMIONE, image species diversity and endemism and are courtesy of NOCS.

28 29 29 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.

28 29 30 DEEP-WATER CORAL ECOSYSTEMS

These coral ecosystems represent an Røst reef off Norway, spanning an area extremely complex and heterogeneous approximately 40 kilometres long by 3 substrate, providing additional hard substrate. kilometres wide. In these environments, These reefs form locally elevated hard structural complexity is a major source of substrates associated with strong bottom heterogeneity. The occurrence of living and currents that enhance food supply. The dead founding species, which determines colonial stone corals Lophelia pertusa and biotic interactions like competition, predation or Madrepora oculata which occur along the chemical defences also play an important role northwestern European continental margin and in habitat partitioning. 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 An example of the extreme complexity of the areas or in fossil systems. Coral mounds are deep-water coral habitats that can be topographic highs build up by the accretion of encountered along the European margins. hard colonial corals and sediments developing Images courtesy of Department for Business, into a complex three-dimensional structure. Innovation and Skills (formerly DTI). The largest coral mound reported so far is the

30 31 31 HYDROTHERMAL VENTS succession of symbiont-bearing bivalves and tube worms, as well as their associated non- Deep-sea hydrothermal vents typically form chemosymbiotic mega-, macro- and black smokers and are biologically more meiofaunal assemblages. Active seepages productive, often hosting complex communities range in scale from about a 100 square metres fuelled by the chemicals dissolved in the vent to 10 square kilometres. These systems are fluids. In the last decade, the discovery of an known from a wide range of European seas extensive hydrothermal field at 30 degrees from the Portuguese continental margins to the north near the eastern intersection of the Mid- Nordic margin, from the Mediterranean Sea to Atlantic Ridge and the Atlantis fracture zone the Celtic margin, at depths from a few (i.e., the vent field named 'Lost City') opened hundred metres to over 4,000 metres. In new scenarios for the exploration of these various cold-seep habitats carbonate crusts systems not only along mid-ocean ridges but and associated fauna were observed down to also on old regions of the oceanic crust away 2,000 metre depth. Mud volcano fields from spreading centres. In hydrothermal vents explored in the Mediterranean (Napoli, Milano, chemosynthetic Archaea form the base of the Urania, Maidstone mud volcanoes) displayed food chain, supporting diverse organisms. The the presence of brines. Submersible dives fauna of Atlantic vents consists for the most allowed identifying large fields of small part of a subset of invertebrate types found bivalves, large siboglinid tube worms, large elsewhere in chemosynthetic ecosystems, with sponges, and associated endemic fauna. taxonomic differentiation usually at the species Several species of bivalves harbouring or genus level. Despite this similarity in bacterial symbionts colonize methane- and taxonomic composition, the ecology of Atlantic sulfide-rich environments. A new species of vents differs from the ecology of Pacific vents Siboglinidae polychaete, the tubeworm in ways that highlight aspects of biogeography, colonizing cold seeps from the Mediterranean trophic ecology and sensory adaptations. ridge to the Nile deep-sea fan, has been While oceanic hydrothermal vents typically recently described. An exceptional diversity of occur at depth over 3,000 metres, most Bacteria lives in symbiosis with small Mytilidae. hydrothermal vents in the Mediterranean with The Mediterranean seeps appear to represent described biological assemblages occur in a rich habitat characterized by megafaunal shallow depths of less than 100 metres. species richness (e.g. gastropods) or the Consequently, a profound difference between exceptional size of some species such as these and the described oceanic deep-sea sponges (Rhizaxinella pyrifera) and crabs vents is the occurrence of photosynthetic (Chaceon mediterraneus), compared with their primary production. Also, the species that background counterparts. The isolation of the inhabit shallow-water Mediterranean Mediterranean seeps from the Atlantic Ocean hydrothermal vents are not endemic to these after the Messinian crisis led to the habitats but represent a subgroup of the most development of unique communities, which are tolerant species in the ambient fauna. The only likely to differ in composition and structure published evidence for deep-sea from those in the Atlantic Ocean. 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

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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.

32 33 33 ABYSSAL PLAINS ANOXIC SYSTEMS

The abyssal plains of the European Seas Numerous deep hypersaline anoxic basins occur typically at depths ranging from (DHABs) have been discovered in the Eastern approximately 3,000 metres (in the Mediterranean Sea, the Red Sea, and the Gulf Mediterranean Sea) to 5,000 metres (in the of Mexico. The six DHABs of the Eastern Atlantic Ocean). Sediments filling the abyssal Mediterranean (L'Atalante, Urania, Bannock, plains are generally dominated by the Discovery, Tyro, and La Medee) are located on deposition of turbidities. These landscapes are the Mediterranean Ridge. These anoxic basins only apparently flat and homogeneous, but lie at depths ranging from 3,200 metres to instead are characterized by the presence of 3,600 metres and contain brine. The seafloor features up to 35 metres in height. In combination of nearly saturated salt addition, biological activities, bioturbation and concentration and corresponding high density excavation by infaunal organisms, as well as and high hydrostatic pressure, absence of the deposition of organic debris and cadavers light, anoxia, and a sharp chemocline makes of pelagic organisms can produce a large these basins some of the most extreme spatial and temporal heterogeneity at different habitats on earth. In these basins a bacterial spatial scales. Typical deep-water groups diversity higher than in the overlying deep include large species contributing to spatial seawater can be found. In the Bannock basin, heterogeneity at small scale, such as five new candidate divisions were also echinoderms, glass sponges, and macroscopic identified in the seawater-brine interface Foraminifera (Xenophyophora). Fishes, through clone libraries. The anoxic layers were decapod crustaceans, mysids, and gastropods dominated by Delta- and Epsilon- are widespread, although much less abundant Proteobacteria. A recent study carried out on in the deep Mediterranean than in the the thermal mud fluids of Urania Basin, northeastern Atlantic. revealed the presence of a highly diverse prokaryotic community, mostly composed of unculturable prokaryotes. Recently, the first OXYGEN MINIMUM ZONES metazoa living in the permanently anoxic conditions were discovered. The sediments of The Oxygen Minimum Zones (OMZs) are L’Atalante basin were inhabited by three bodies of water where dissolved oxygen species of the animal phylum Loricifera concentrations fall below 0.5 to 0.2 ml.L-1. (Spinoloricus nov. sp., Rugiloricus nov. sp. and Where an OMZ impinges on the seafloor, Pliciloricus nov. sp.) new to science. 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.

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

32 33 34 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.

34 35 35 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

34 35 36 PRESERVING HABITAT DIVERSITY regions, action is needed now to preserve AND HETEROGENEITY biodiversity before that this is lost. A possible solution for the conservation of the hot spots of

Hot-spot ecosystems are typically biodiversity is applying the precautionary characterized by high habitat/topographic principle to protect the deep-sea areas around complexity. These hot spots, bearing a higher EU margins and islands that are biodiversity than other deep-sea ecosystems, topographically highly complex and typically support higher levels of ecosystem heterogeneous. This action would be certainly functioning and efficiency. Since most of the beneficial for preserving the associated seafloor is still unexplored, while biodiversity and is extremely important for the anthropogenic impacts leading to habitat sustainability of deep-sea ecosystem destruction or homogenization (e.g. trawling) processes. are extending even to the most remote marine

36 37 37 Biodiversity in European Seas

CUMULATIVE KNOWLEDGE The discovery of new marine organisms The study of marine biology has a long history continues apace – with an average of about in Europe and the diversity of marine 1,500 new species described globally each organisms is probably more comprehensively year over the past 20 years. These range from documented for European waters than microbial end of the size spectrum, such as anywhere else on Earth. After well over two Archaea and bacteria, up to vertebrates, but centuries of detailed exploration we know, with the great majority of newly described species a high degree of accuracy, that in the year comprises multi-cellular invertebrates. 2000 at least 29,714 species of marine Although European waters are relatively well organisms had been recorded from European studied, new species are continually being seas. Almost all animal phyla occur in the recognised there: since 2000, species new to oceans, so diversity in basic body organization science have been added to the European is high, but species richness is not evenly Register of Marine Species spread across all marine groups. The top (www.marinespecies.org) at a rate of just over dozen dominant taxa in Europe comprise over 50 per year. Including the species described 25,500 species, over 85% of the total (p.39). that originate from outside of Europe but have either been found in, or have spread into, The largest taxon is the Crustacea which, with European waters in the past decade, adds 7,137 European marine species, is more than further to the regional fauna. The total number twice the size of the next most species rich of marine species for Europe is now group, the Mollusca, with 3,353 species. The approaching 32,000 and represents nearly next three groups are all worms of different 14% of global marine diversity, estimated by kinds. The flatworms comprise the third largest Bouchet as approximately 230,000 species. taxon within the European marine fauna with 2,398 species. Over half of them are parasites, either gill flukes (Monogenea) or intestinal NEW MICROBES flukes (Digenea), or tapeworms (Cestoda). Next are the annelids (2,160 species), The discovery of new species is often comprising the free-living polychaetes and dependent on the use of new technology or oligochaetes, plus the leeches. Then we have new investigation tools. This is especially true the nematodes. Free-living nematodes are of the microbes which can be extremely both abundant and species rich, but the abundant, with one million bacteria in a single diversity of marine benthic nematodes is poorly one millilitre drop of sea water, and can exhibit represented in checklists since only a small high diversity, with up to 10,000 bacterial proportion of the estimated total number of species per millilitre. Since scientists cannot species has been described and named. identify most microbes by their external Parasitic nematodes are common in marine appearance, they have to rely on molecular metazoan hosts but comprise a relatively small methodologies to describe their diversity. A part (12%) of total nematode count (1,837 standard method is to study the ribosomal species) in European seas. genes, in particular the so-called 16S and 18S ribosomal ribonucleic acid genes, which are The macroalgae are the sixth most abundant extremely stable gene subunits, providing group, although this grouping is an artificial information that corrupts only slowly through assemblage of red, brown and green algae. geological time scales. Determining the They are followed by the sponges (1,640 genetic code (the base sequences) in these species) and then the fish (1,349 species) and genes provides insight into the evolutionary cnidarians (1,329 species). In the eighth place relationships and therefore the classification of are the foraminiferans (1,167 species), the organism, as well as insight into its followed by the Bryozoa (724 species) and the functional properties. dinoflagellates (718 species). Just dropping out of the top 12 are familiar but relatively low The red bacterium Rhodopirellula baltica (p.39) diversity groups such as the echinoderms (648 was originally isolated from the Baltic Sea but species) and the tunicates (481 species). was thought to occur widely in the seas around Europe. However,

36 37 38 Crustacea Mollusca Platyhelminthes Annelida Nematoda Macro-algae Porifera Fish Cnidaria Foraminifera Bryozoa Dinoflagellates

The dozen most diverse groups of marine organisms in European seas

A B

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.

38 39 39 characterization of the bacterium on the our knowledge of the host specificity of the genetic level, using 16S rRNA, revealed a parasites, their abundance, and their cluster of species within the genus distribution in European waters. There is even Rhodopirellula. Using a technique called whole an as yet unnamed new parasitic copepod genome hybridization it was shown that (p.41) which lives on the sabellid polychaete Rhodopirellula baltica was actually restricted to Jasmineira caudata. The copepod body is the Baltic Sea, the Skagerrak and the eastern transformed into a globular trunk which carries North Sea. The majority of the isolates egg sacs, but its anterior end penetrates the obtained belonged to a second species body wall of its host. The unusual features of present in the English Channel, on the French this parasite exclude it from all known families Atlantic coast, and in the Mediterranean. A and it may represent an entirely new family third species was found in North Atlantic from European waters. habitats around Iceland and Scotland and a fourth species in the Adriatic Sea. The One of the generally under-explored sectors of presence of four species of Rhodopirellula in multi-cellular animal diversity is the parasites. European seas shows considerable Marine fishes serve as both intermediate and evolutionary diversification within the genus. final hosts to a wide diversity of flatworm and Rhodopirellula baltica was the first other parasites in European waters and the planctomycete bacterium to have its genome fauna remains incompletely known, especially completely sequenced, and transcriptional in deep water. Specimens of the short-fin profiling confirmed that R. baltica is highly spiny eel Notacanthus bonaparte caught at responsive to changes in its environment. This depths in excess of 1,000 metres on the makes R. baltica ideal to serve as a model Goban Spur had intestinal flukes which were organism, but only if the species is correctly described as a new genus and species of identified. digenetic fluke, Steringovermes notacanthi, by Bray. Many digeneans are specific in their choice of host and Steringovermes notacanthi NEW INVERTEBRATES is named after its notacanthid host.

Higher up the size spectrum are the copepods Invertebrates also have parasites, although - diminutive relatives of the crabs and lobsters, less is known about them than parasites of but abundant and diverse in the oceans. There vertebrate hosts. The separate subclass status are about 3,000 species of copepods in of microscopic parasites called tantulocarids European waters, and they comprise about was first recognised in the 1980s and these 10% of all species contained in the European parasites continue to be discovered on various Register of Marine Species. Free-living marine crustacean hosts in the oceans of the copepods are typically the dominant group of world. They occur throughout European seas multi-cellular animals in the plankton but they but are rarely reported because of their small also live on and in marine sediments where size. The most recent addition to the fauna is they are usually second in abundance only to Microdajus tchesunovi from the White Sea, the nematodes. Copepods are also parasitic which was described only in 2010. The larval on hosts representing almost every phylum stage of Microdajus is only 100 microns in from sponges to chordates, including whales. length and is attached to its tanaid host by means of an adhesive oral sucker (p.41). Several families are parasitic on polychaete worms but these parasites are typically rare Newly discovered in European waters is the and our knowledge of their biology and crustacean subclass Cephalocarida, which distribution has been extremely limited. Such have often been considered to be the most parasites are usually found by researchers known primitive crustaceans. The species, studying the hosts so the sheer amount of Lightiella magdalenina, was originally known macrobenthic sampling and analysis that has from a very restricted site, about 15–20 metres taken place within the past decade has deep on the southern shore of a tiny island in provided an exciting opportunity to collect the La Maddalena Archipelago, off Sardinia, these very rare animals. The diversity of new but it has since been found off the coast of forms found was astonishing: in a large series Tunisia. 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

38 39 40

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

40 41 41 GENETIC STUDIES AND CRYPTIC SPECIES Two forms of the phyllodocid polychaete Notophyllum foliosum were known to occur in Biodiversity describes the variety of life at all Scandinavian waters. There was a deeper scales from genes to ecosystems and modern water form that was palish yellow to grey in molecular genetic methods have enabled us to colour, with black patches, and a shallower study fine scale, within-species variation. Such form that was yellow-orange with black approaches have dramatically improved our patches and white spots. The deeper form was knowledge of the complex structure of marine often associated with reefs of the deep-water fish populations and their adaptations to coral Lophelia pertusa. Using two different environmental gradients and local conditions. genes, recent analysis showed that these two This knowledge helps us to analyse the forms represent different species and the environmental basis for spatial structure in fish deeper form was formally named Notophyllum populations, and examine how the spatial crypticum. distribution of local populations changes over time. The new methodologies have been The species complexes discovered for applied to marine species such as cod, Echinocardium cordatum and for Notophyllum herring, and sprat throughout the salinity are just two examples of the widespread gradient in the North Sea – Baltic Sea area. phenomenon of cryptic speciation. Cryptic These analyses showed that the steepest species can arise when genes and morphology gradient in genetic variation largely coincided evolve at different rates, so they have spatially with the steepest gradient in salinity undergone rapid genetic evolution leading to (i.e. in the western Baltic Belt Sea area), and reproductive isolation, but this is not reflected that populations in the Baltic were genetically in similarly rapid morphological changes. distinguishable from those in the North Sea. In Discovering and documenting this hidden the case of the sprat, Sprattus sprattus, the biodiversity is a major challenge for marine existence of isolated genetically distinct biologists. populations has been demonstrated in the northern Mediterranean basins and they remain isolated because of their inability to EXTREME ECOSYSTEMS maintain gene flow in the currently warmer oceanographic regime in the Mediterranean. The exploration of extreme ecosystems, such Such advances in knowledge of fish genetics as marine caves, has provided some notable can help improve the way fisheries are discoveries. Such caves provide a managed and inspected, including efforts to permanently dark, stable, quiescent prevent illegal fisheries. environment with limited food resources that offers some parallels with the deep sea. In the The genetic analysis of marine organisms has north-western Mediterranean one particular shown various examples of cryptic species, i.e. cave, the 3PP cave near Marseille, has a populations previously thought to belong to the descending profile that traps cold water (~13- same species because of a lack of 15°C) all year round and the deep interior of morphological diagnostic characters. The heart the cave shows strong faunal and ecological urchin Echinocardium cordatum, for example, parallels to the deep sea. One of the most is found from the North Atlantic to the Pacific, striking and best studied examples is the including the Mediterranean. Because its carnivorous sponge Asbestopluma hypogea development includes a planctotrophic larva (p.43). This belongs to an exclusively bathyal stage which confers a high dispersal potential, and abyssal sponge family, the Cladorhizidae, it has been treated as a single widespread but is found in dense populations at 15-25 m species. Recent genetic studies have shown depth in particular caves. The same caves can that E. cordatum (p.41) is a species complex also harbour the fragile hexactinellid glass consisting of five different clusters, separated sponge Oopsacas minuta, normally found by clear genetic discontinuities which in turn between 300 and 3,000 metres in the deep provide strong evidence of reproductive Mediterranean. These descending cold-water isolation and therefore speciation. Three of caves are home to an interesting mixed marine these clusters (clades) exist in European cave fauna, successfully established true waters: one restricted to the Atlantic, a second deep-sea species, and an additional ranging from the Atlantic off Galicia into the consortium of mobile shallow-water taxa using Mediterranean, and a third restricted to the caves as shelter from predators. Mediterranean. The other two clades are North and South Pacific.

40 41 42 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.

42 43 43 Other extreme habitats that have provided rich Carlos Ribeiro mud volcano was described by sources of new species in recent years include Hilário and Cunha under the name hydrothermal vents, cold seeps, gas hydrates Bobmarleya gadensis. This splendid name and mud volcanoes. The mud volcanoes in the pays tribute both to the “shape of the Gulf of Cádiz, first discovered in 1999, are tentacular crown in which tentacles largely inhabited chemosynthetically-based resemble dreadlocks, a hairstyle popularised communities dominated by frenulate worms by the reggae singer and songwriter Bob (members of the polychaete family Marley”, and to the proximity of Cádiz (the Siboglinidae). One new frenulate (p.43) name of which was Gades in Roman times). discovered at a depth of 2,200 metres on the

42 43 44 Alien Species

ORGANISM GROUPS TERMINOLOGY Marine alien species represent extremely broad taxonomic spectrum of aquatic free- Non-indigenous (alien, exotic, non-native) living and parasitic organisms, including species are species or lower taxa introduced bacteria, plants, animals, fungi and other outside of their natural range and dispersal organisms. Amongst bacteria, for instance, the potential. This includes any part, gamete or Vibrio cholera bacteria has been dispersed by propagule of such species which might survive sea going vessels. Amongst plants, green, red and subsequently reproduce. and other algae (e.g., diatoms and Invasive alien species are a subset of dinoflagellates); mosses, liverworts and established nonindigenous species which have hornworts; and flowering plants have been demonstrated their potential to spread recorded as alien species. Amongst animals, elsewhere and have adverse effect(s) on several representatives of the following taxons invaded regions. have been recorded as aliens: annelids, bony and cartilaginous fish, bryozoans, Cryptogenic species are those of unknown chaetognaths, cnidarians, crustaceans, origin which cannot be defined as being native echinoderms, insects, molluscs, nematodes, or alien. sea squirts and sponges. Introduction is either intentional or unintentional human-mediated dispersal of nonindigenous species. Secondary INVASION SUCCESS introduction of nonindigenous species from the area(s) of their first arrival could occur without Higher potential to become an alien is shown human involvement due to spread by natural by species with high abundance in native means. habitat, ability to survive during the introduction process, wide range of habitat selection, high Biological pollution (biopollution, bioinvasion tolerance to abiotic factors, wide food impact) is the impact of invasive alien species spectrum, high reproduction rate, fast growth, at the level that disturbs ecological quality by alien status elsewhere, potential to replace having effects on individual, population, native species, long-lasting larval stage, community, habitat and ecosystem levels. pelagic life-history stage and ability to produce resting stages.

Introduction hot spots are areas with matching ORIGIN IN EUROPE hydroclimate (i.e., temperature and salinity) between the destination and source region. In Non-indigenous marine biota in different addition, the following characteristics of the European seas originates from diverse source destination area are important: availability of areas. Some species have been introduced ‘ecological niche’, low abundance or absence from distant overseas regions (e.g. south- of predators and parasites, strong eastern Asia, Australia, New Zealand, anthropogenic influence, low native species Americas), while others from one region of diversity. 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.

44 45 45 Green macroalgae Caulerpa racemosa var. cylindracea. Image courtesy of M. Cormaci.

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

44 45 46 TRANSPORT PATHWAYS Red Sea species through the Suez Canal into (WITH EXAMPLES OF MAIN the Mediterranean (commonly referred to as Lessepsian or Erythrean immigration). VECTORS) Estimates of the number of Erythrean immigrant metazoan species vary from 558 to • Ships: ballast water and sediments, hull 903, with the disparity largely due to different fouling, intakes and crevices, bored wood, authentication protocols between studies. bilges and ships water, anchor and anchor Despite the uncertainty over the precise chains, lockers fenders, portable moorings, number of immigrants, the influx continues deck recesses, dredge spoil and sediment apace and the scale of the problem has led to displacements; the recognition by the European Environment • Canals: water flow, tidal exchanges, and Agency (EEA, 2006) of biological invasions as other alteration to water levels from lock one of the priority issues of concern to the flushing, transport of floating timber, health of Mediterranean marine ecosystems. pontoons; • Wild fisheries: stock movements, Changes to the Eastern Mediterranean fish population re-establishment, discards, fauna have been particularly visible and the disease agents from fish processing, live populations of some immigrant species have bait releases and discharges of live grown to the point where commercial fisheries packaging material, movement of retrieved have been established to harvest them. fishing equipment, releases of organisms Immigrant species of Red Sea clupeids such intended as living food supplements, as red-eye round herring Etrumeus teres for releases of transported water; example, are important in inshore-pelagic • Culture activities: intentional releases fisheries off the Egyptian coast. There have and movement of stock associated water, been few studies of the parasites of these movement of gear, discarded or lost gear, immigrant fish, but recently the gill parasitic live packaging materials and/or associated copepod Mitrapus oblongus has been transport media, release of genetically discovered in the Mediterranean for the first modified species; time. This parasite originates in the Indo- • Aquarium and live food trade: intentional Pacific but has been carried into the and accidental releases from aquaria, Mediterranean via the Suez Canal on its Red untreated waste discharges, unauthorised Sea immigrant host. The alarming discovery releases of imported living foods, here is that Mitrapus oblongus was also found discharged live packaging materials, on the gills of a native Mediterranean clupeid releases of transported water; fish, the sardine Sardinella aurita. This is the • Leisure activities: live bait movements, first documented case of host switching of any discharge of packaging materials, metazoan parasite from a Red Sea immigrant accidental/ intentional transport and to a native fish host. The potential impacts of release of angling catch, water sport such host switching events on the populations equipment, stocking for angling; of native hosts are profound, especially when • Research and education: intentional and the hosts are the subject of important fisheries. accidental release, wastewater and Alarmingly, at least four more Red Sea biological waste discharges, discarded parasitic copepods have since been found in samples, releases from cultures, gear the eastern Mediterranean. movement, releases/ escapes of caged organisms; • Biological control: releases to control THREATS AND BENEFITS invasive species; • Habitat management: soil Invasive alien species might threaten humans, stabilization/reclamation, sediments and cause adverse effects on environmental quality plantings, use of filter-feeding and cause damage to economies. However, invertebrates for managing water quality. 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: INVASIVE SPECIES Cholera is one of the best known fatal diseases. Caused by various strains of Vibrio The marine fauna of the Eastern cholera bacteria, symptoms of the disease Mediterranean is undergoing a profound and vary from mild to acute diarrhoea accompanied rapid change due to sustained immigration of

46 47 47 Green macroalgae Codium fragile. Image courtesy of E. Ballesteros.

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

46 47 48 by abdominal cramps, nausea, vomiting, THREATS dehydration and shock. The planktonic dinoflagellate Alexandrium catenella which • Human health; occures in several European regional seas, is • Changes in resource competition (food, responsible for creating ‘red tides’ and space, spawning/nursery areas) producing paralytic shellfish poisoning (PSP) • Changes in habitat (chemical, such as use toxins which can affect humans, other of biocides; physical, such as reduced mammals, birds and fish. water movements; biological); Ecological impacts: Impacts of alien invasive • Limitation of resources (e.g., space, species have been recorded at genetic, nutrients, light, oxygen); species, community and ecosystem levels. • Introduction of new functional groups and These might range from simple interactions changed foodwebs; between non-native and native species to • Uncontrolled dispersal through massive shifts at biotope level resulting in unexpected ecophysiological response; altered ecosystem functioning. Alien invasive • Introduction of potentially toxin producing species can also act as ecosystem engineers, species (harmful algal blooms, some influencing the habitat itself, positively or seaweeds); negatively, directly or indirectly (see sections • Introduction of disease agents or parasites on threats and benefits below). (viruses, bacteria, fungi, ecto- and Examples of economic losses: Invasion of endoparasites) associated with an alien species may result in significant introduced host species; economic losses for shipping industry, fishery • Genetic effects on native species and tourism. In addition, they may cause harm (hybridisation, change in gene pool, loss to culture and aesthetic value of oceans. The of native genotypes); Ponto-Caspian zebra mussel (Dreissena • Reduction or extinction of native polymorpha) is perhaps one of the most populations; ’famous’ examples of bioinvasions. It is • Alterations of native communities; primarily a freshwater species, but lives in • Introduction of a species being a missing brackish ecosystems. It was unintentionally link as host in the life cycle of parasite; transported to the North American Laurentian • Effects on underwater constructions by Great Lakes in the 1980s. Since then, and fouling alien species (water intakes of through significant and devastating impacts on power plants and urban water supplies, several abiotic and biotic ecosystem boats), expensive cleaning procedures properties, fishery and infrastructure, the and application of preventive measures estimated financial damage in the US was up (antifouling paint); to one billion dollars. The predatory comb jelly • Tourism (accumulation on shores causing (Mnemiopsis leidyi) was accidentally smell or sharp shells that have to be introduced via ship ballast water to the Black removed, dense growth in shallow bays Sea in the early 1980s. In its new predator-free used for swimming); habitat, the jellyfish colonised the entire • Loss of commercial or recreational fishery; ecosystem and through trophic interraction (by • Losses of aquaculture harvest; predating on zooplankton, fish eggs and • Cost of chemicals for eradication; larvae) disrupted the foodweb and contributed • Damage caused to underwater heritage to collapse of the local fishery resources with objects such as sunken sailing vessels; monetary damage of several hundreds millions • Shoreline erosion; dollars. The small phytoplankton alga • Recreational value; Chattonella cf. verruculosa produces toxin • Aesthetic and artistic values. 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 Examples of economic benefits: Alien killed 350 tonnes of farmed Norwegian salmon. 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

48 49 49

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

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

48 49 50 1960. Although Pacific oysters directly Through simulations of a coupled model of introduced from the wild have been source of bioenergetic-based anchovy population several cryptic diseases, and uncontrolled dynamics and lower trophic food web structure harvests of oysters contaminated by it became evident only recently how interaction microbiota can lead to diseases of humans, of different factors resulted in the this species is now responsible for the main unprecedented 1989–90 anchovy–Mnemiopsis biomass of mollusc production in Europe. shift in the Black Sea. It appeared that combination of the density dependent effects of overfishing, eutrophication-induced nutrient BENEFITS enrichment, climate-induced over-enrichment and temperature-controlled Mnemiopsis spring • Stock enhancement; production were jointly involved in the shift. • Provide organic material, nutrients and food; Knowledge gap: The assessment of genetic • Increase in biodiversity; impacts of alien species on native organisms is • Increase of bioturbation and oxygen a relatively new field of research. It has been availability (including oxygen production); possible since relatively recently to detect genetic changes at the level of single genes. • Better conditions for denitrification (shunt Therefore, perhaps the most understudied for eutrophication); impact of alien species may be the genetic • Increase in water transparency; impacts they have on native biota. Today, the • Storage of nutrients; knowledge on changes in the genetic integrity • Shelter or settling substrate for several of indigenous populations resulting from alien native species; species introductions and genetically-modified • Protection of shoreline against erosion and organisms is mainly limited to hybridization flooding; events. • Decreased numbers of previous introductions; • Scientific and educational information; INTERNATIONAL COOPERATION • Improved fishery harvest of wild catches or aquaculture; Conventions, organisations and • Management of coastal areas; regulations: The United Nations Convention • Bioremediation and biofilters; on the Law of the Sea (UNCLOS) explicitly • Increased employment. places a general requirement for parties to take measures “to prevent, reduce and control pollution of the marine environment resulting ACHIEVEMENTS AND GAPS from…the intentional or accidental introduction of species alien or new, to a particular part of Two examples of application of new the marine environment, which may cause methodologies: Traditional taxonomic significant and harmful changes thereto” analysis and approaches have proven non- (Article 196). satisfactory not only in assesseing biodiversity, but also in taxonomic identification of alien The Convention on Biological Diversity species and studies of their likely area of (CBD) sets commitments for maintaining the origin. Molecular tools offer rapid and accurate world’s biological diversity with three main means to obtain reliable infromation in these goals: conservation of biological diversity, aspects. There are several recent examples on sustainable use of its components, and fair how these approaches have been applied. For and equitable sharing of the benefits from the instance, nucleotide sequence analysis of use of genetic resources. Article 8h of the ribosomal RNA (rRNA) was used for Convention calls on parties to prevent the taxonomic identification of ctenophores introduction of, control, or eradicate those alien collected in the northern Baltic Sea, where species that threaten ecosystems, habitats or alien Mnemiopsis leidyi and the native species. Pleurobrachia pileus have been reported to occur. The genetic analysis showed that, The Global Invasive Species Programme contrary to previous reports, there was only (GISP) is an international partnership with the one specie called Mertensia ovum, a aim of conserving biodiversity and sustaining ctenophore with a broad Arctic and livelihoods by minimising the spread and circumboreal distribution, which has never impact of invasive species. It provides support been reported to occur in the Baltic Sea.

50 51 51 Zebra mussel Dreissena polymorpha. Image courtesy of J. Kotta.

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

50 51 52 to the implementation of Article 8(h) of the ICES Code of Practice on the Introduction CBD (http://www.gisp.org). and Transfers of Marine Organisms. It follows the precautionary approach adopted International Convention on the Control from the FAO principles, with the goal to and Management of Ships’ Ballast Water reduce the spread of exotic species. It and Sediments (BWMC): The main goal of accommodates the risks associated with the of the International Maritime Organisation current commercial practices including trade of (IMO) is to prevent, minimize and ultimately ornamental species and bait organisms, eliminate the transfer of harmful aquatic research, and the import of live species for organisms and pathogens through the control immediate human consumption. It also and management of ships' ballast water and includes species that are intentionally imported sediments. to eradicate previously introduced invasive species, as well as genetically modified The EC "Regulation for use of alien and locally organisms and polyploids. It outlines a absent species in aquaculture" (EC, 2007) consistent, transparent process for the establishes a system for assessment and evaluation of a proposed new introduction. management of the risks associated with the introduction of new organisms for aquaculture.

Helsinki Convention (HELCOM): As a part of RESEARCH FRAMEWORKS the HELCOM Baltic Sea Action Plan (BSAP), the road map towards ratification and Several aspects of biological invasions were harmonized implementation of the BMWC was considered in a number of recently completed adopted in 2007. According to BSAP, EU framework projects. These are: HELCOM countries agreed to ratify the BWM DAISIE: Inventory of all known alien species in Convention as soon as possible, but by 2013 Europe and identification of the top 100 ‘worst’ at the latest. invaders, their distribution and spread. This Oslo-Paris Convention (OSPAR): The project summarised the ecological, economic Quality Status Report 2010 will provide an up- and health risks and impacts of the most to-date evaluation of the marine environment significant species (http://www.europe- of the North-East Atlantic, summarising ten aliens.org/). years of assessment work under the OSPAR. ALARM: Management of alien species with Nonindigenous species are identified as a the development of toolkits and relevant pressure of human activities in the recommendations in terms of environmental OSPAR Maritime Area. policy, the interaction of invasive alien species Barcelona Convention: Nonindigenous and sociology, climate change and chemicals. species and their impacts are considered in One of the project’s products was the the context of protected areas. The protocol development of the biopollution assessment concerning the Mediterranean Sea as a system (http://corpi.ku.lt/~biopollution/). specially protected area obliges Parties to take IMPASSE: Development of guidelines and measures in order to protect these areas. The policies for environmentally sound practices for measures may include the prohibition of the introductions and translocations in aquaculture introduction of exotic species and the that also covers quarantine procedures as well regulation of the species introductions in as risk assessments and assesses the impacts protected areas. of invasive alien biota in aquaculture, protocols The International Council for the and procedures for assessing the potential Exploration of the Sea (ICES) noted the risks impacts of invasive alien species in associated with uncontrolled species aquaculture and their economic impact introductions and transfers almost 40 years (http://www.hull.ac.uk/hifi/IMPASSE). ago. Today ICES has two working groups to MARBEF: Network of excellence, consisting of address the issue, i.e. the ICES Working almost 100 European marine institutes, a Group on Introductions and Transfers of platform to integrate and disseminate Marine Organisms (WGITMO) to deal with the knowledge and expertise on marine movement of NIS for e.g. aquaculture biodiversity, with links to researchers, industry, purposes and the ICES/IOC/IMO Working stakeholders and the general public Group on Ballast and Other Ship Vectors (www.marbef.org). which focuses on species movements with ships.

52 53 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.

Fi 52 nding new life. References

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