Marine Biodiversity the Rationale for Intervention

www.defra.gov.uk

Marine Biodiversity The rationale for intervention

Building the evidence base for the Marine Bill

July 2006

Marine Biodiversity The rationale for intervention

Chris Frid & Odette Paramor

School of Biological Sciences, University of Liverpool, Crown Street, Liverpool, L69 7ZB

Disclaimer: The content of this report does not necessarily reflect the views of Defra, nor is Defra liable for the accuracy of information provided or responsible for any use of the reports content.

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Executive Summary

As an island nation, the seas have a large cultural significance for the peoples of the British Isles. They have also had a significant role in the UK economy, as a mode of transport for trading, as a provider of food resources and as a means of disposing of waste. The scale and nature of how the seas are used has changed over time, and it is now recognised that man’s actions can impact the way the marine system works, and that one use may compromise the fitness of the seas for other purposes. The University of Liverpool was commissioned by Defra (CRO 0359) to provide a short evidence-based report to support the development of policies to improve the conservation of marine biodiversity by detailing:

• the importance of marine biodiversity, the current status and trends in the UK’s marine biodiversity; and • for any decline, loss or deterioration what the likely consequences for the delivery of ecosystem goods and services.

While the waters around the UK may be well studied, the general conclusion from Charting Progress (2005)[1], which reviewed of the state of the UK seas was that data, particularly for offshore areas, tended to be sparse or non- existent, and that data on long-term or broad spatial scales were rare, resulting in evidence for change often being inconclusive. Even for comparatively well studied systems, such as grasslands, there is still considerable uncertainty as to the nature of relationships between ecological functions and biological diversity. As such there is even less confidence in the nature of such relationships for marine systems.

Given these difficulties, a pragmatic approach has been adopted for the purposes of this study. A body of ecological theory, models and experimental data are available, and the understanding of system functioning that is emerging allows some, tentative conclusions to be drawn. However, given that these are all tentative conclusions they should be used to develop management measures which are both ‘precautionary’ and form part of an ‘adaptive management scheme’. Management can then be reviewed regularly and adjusted based on new scientific understanding and evidence, gathered from monitoring the management measures ability to deliver its objectives.

The total marine Exclusive Economic Zone (EEZ) claimed by the EU extends to 11,447,075km2. The three largest national contributors are Ireland (890,688km2, 7.8%), the UK (867,000km2; 7.6%) and Spain (683236 km2, 6.0%). Portugal is the only other nation with oceanic and coastal seas. Therefore the UK has both a significant proportion of the total European seas and is responsible for a large part of the oceanic component of the European EEZ. Maritime activities contribute about 5% of the UK GDP. While it is impossible at this time to partition direct and indirect economic benefits derived from marine goods and services provided by the European seas to any particular sea area, there is a good basis for considering the UK’s EEZ to be very important in the European context.

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In addition to these direct uses of the marine environment, the sea provides many indirect benefits: • it is a major reservoir of biological diversity with over 44,000 species recorded • it is a major store of the greenhouse gas carbon dioxide (CO2) and assists in regulating the earth’s climate. • organisms in the sea play a vital role in nutrient recycling, returning nitrogen, phosphorus and sulphur to the biologically active part of the global ecosystems.

The report considers ecological goods and services in the marine environment under 6 broad categories: • atmospheric gas assimilation and climate regulation • nutrient recycling • changes to waste assimilation capacity • habitat functions • food provision • biodiversity for society (i.e. recreation: angling, bird watching, boating, coastal visits and diving, existence and cultural values)

For each category of ecological goods and services, the ecosystem components (plankton, benthos, fish, birds, marine mammals etc) that contributed to its delivery were identified and evidence of changes in the status of those ecological components was documented. Where changes had occurred we also considered the extent to which the observed changes might compromise delivery of the ecological services.

Summary of the analysis of the evidence that biological systems that delivery ecological services have been compromised and the risk to the continued delivery of the service

Ecological services Quality of evidence of a Risk to delivery of deterioration in ecological service ecosystem providers Gas and climate regulation Good Low-moderate Nutrient cycling Some Low Waste treatment Good Low (Moderate for nutrient containing wastes) Habitat functions Good High Food and material provision Good High Biodiversity in support of Good High societal values

Following the consideration of the current evidence for changes in the biological systems that deliver the ecological goods and services, it was found that: • there is good evidence of deleterious change in many of the marine ecosystem components. Thus both biodiversity, and the ecological functions that the marine environment provides, are being altered as a result of human activities; • the highest risk of a failure in system functioning would result from changes in the microscopic organisms that live in the water (the plankton), the organisms inhabiting the sea floor (the benthos) and the deterioration of the habitats on which they depend. These groups provide the food resource for all other components but also deliver key services through waste treatment and assimilation, nutrient cycling and atmospheric gas regulation; and • a diverse range of recreational activities, of considerable economic value (£11.7 billion, Beaumont et al. unpub.), are dependent on the higher trophic levels, so while loss of these groups may not greatly impact delivery of most ecosystem functions, they would compromise some of the economic benefits gained from the UK’s seas. Human activities which influence large-scale patterns will have the greatest effects. In particular, anthropogenic climate change. Increasing temperatures, increased storminess, acidification of seawater are all likely to have effects far beyond those resulting from localised disturbances such as fisheries, aggregate extraction and waste disposal. The latter may however be locally important, especially when they occur in unique or rare habitats.

Contents

Executive Summary iii

Chapter 1 - Introduction 1

1.1 Aims 2 1.2 Approach adopted 3 1.3 Report structure 3

Chapter 2 - Species, habitats and ecosystem processes important for the supply of ecosystem goods and services to the UK 4

2.1 The supply of ecosystem goods and services 4 2.2 Assigning importance to ecosystem components 5 2.3 Assigning importance to ecosystem goods and services 5 2.3.1 What are ecological functions ? 5 2.3.2 Nutrient recycling 8 2.3.3 Atmospheric gas assimilation and climate regulation 8 2.3.4 Capacity for waste assimilation 8 2.3.5 Habitat functioning 9 2.3.6 Food provision 9 2.3.7 Societal value of biodiversity 10 2.4 The importance of the UK’s seas in global and European context 11

Chapter 3 - Evidence of status and trends in UK marine biodiversity 14

3.1 Important ecosystem goods and services 14 3.1.1 Atmospheric gas assimilation and climate regulation 14 3.1.2 Nutrient recycling 14 3.1.3 Waste assimilation capacity 15 3.1.4 Habitat function 17 3.1.5 Food provision 17 3.1.6 Biodiversity for recreation, existence and cultural values 19

Chapter 4 - Assessment of risk to the supply of important goods and services 20

4.1 Timescale for changes 20 4.2 Risk evaluation for atmospheric gas assimilation and climate regulation 22 4.3 Risk evaluation for nutrient recycling capacity 23 4.4 Risk evaluation for loss of waster assimilation capacity 23 4.5 Risk evaluation for habitat functions 23 4.6 Risk evaluation for food provision 24 4.7 Risk evaluation for biodiversity in support of societal values 25

Chapter 5 – Concluding remarks 27

Acknowledgements 29

References 30

Appendices Appendix 1- Species of Importance 46 Appendix 2 - Trends in the important species and groups of species 51

List of Figures Figure 1 The distribution of marine landscape features in UK seas Figure 2 Long term monthly variability of Phaeocystis from CPR records averaged from the North Sea Figure 3 Total estimated grey seal pup production for all major breeding colonies in Scotland and England (excluding Loch Eriboll, Helmsdale and Shetland) from 1984 to 2002. Estimates are within ± 14% of the point estimates Figure 4 Trends in the kittiwake breeding success EcoQ metric determined for between 2 and 7 colonies along the east coast of Scotland between Troop Head and St Abbs and sandeel catch from the closure area Figure 5 Long-term trends in the utilisation of the 0 group and 1+ group sandeel resource by industrial fisheries and fish and seabird predators based on data derived from the MSVPA

List of Tables Table 1 Categories of ecosystem goods and services as defined by Costanza et al. (1997) for their global environmental valuation, and by Beaumont and Tinch (2003) for their analysis for the UK seafloor and their relationship to the groupings used in this report1 Table 2 The quantity and value of UK fish and shellfish landings 2000-2004 Table 3 Recreational participation and club membership levels Table 4 Turnover and ‘Value Added’ by the marine sector in the UK economy. Re-valued to 1999 prices, all £ million Table 5 Definitions of standard terms used to define the quality of the evidence for changes in critical ecosystem components and the associated risk to delivery of ecosystem goods and services Table 6 Summary of the analysis of the evidence that biological systems that delivery ecological services have been compromised and the risk to the continued delivery of the service Table 7 The status of cetacean species occurring regularly in UK waters

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Chapter 1 - Introduction

1.1 As an island nation, the seas have a large cultural significance for the peoples of the British Isles. They have also had a significant role in the UK economy; as a mode of transport for trading, as a provider of food resources and as a means of disposing of waste. The scale and nature of how the seas are used has changed over time, and it is now recognised that man’s actions can impact the way the marine system works, and that one use may compromise the fitness of the seas for other purposes. Modern systems of environmental management seek to use holistic and integrated approaches to management. These management approaches recognise that changes in one part of the environment, such as winter sea temperatures, may affect another part of the system, for example fish breeding, and that different human activities also interact with each other.

1.2 Economic terminology refers to the benefits the environment provides society with in terms of ‘ecological goods and services’. We can think of things, such as the catch of fish, aggregates, and energy as ‘goods’, and processes, for example the breakdown of sewage into nutrients and the dispersal of pollutants, as ‘services’. However, the boundary is not absolute nor particularly important. A sea without any living organisms could still supply some goods and services but a very restricted set. Therefore to ensure that the people of the UK have seas that deliver their cultural needs and meet the demand for goods and services requires functioning biological systems.

1.3 Pristine marine systems would deliver, by definition, natural levels of goods and services. However by using these goods and services, the system is moved away from a pristine state. Thus it is critical to identify the extent to which the functioning of marine ecosystems can be altered without compromising their ability to deliver desirable goods and services. In doing this, society may decide that the economic benefits that accrue from a particular action outweigh the loss of ecosystem goods and services. However, we should make this an informed choice and not a consequence of poor management.

1.4 Defra is currently considering a number of provisions as part of the proposed Marine Bill to improve marine nature conservation. The University of Liverpool were commissioned by Defra (Contract Reference CRO 0359) to provide a fully reference desk-based review that describes the UK’s marine habitats, species and ecosystem processes, place them in a European context and summarises any evidence of changes in trend and status. The implications of such change on the state of the marine ecosystem, and its ability to provide the goods and services which are relied upon was also considered.

1.5 This report presents the output of this study and seeks to identify the habitats and species which contribute most to the delivery of the ecosystem services provided by the UK marine environment. Given the timescales for delivery and available resources it was not feasible to consider all habitats and species, nor to consider all individual goods and services. Rather the

1 report seeks to consider the principle groups of ‘goods and services’ (Chapter 2) and examples of the habitats and species that contribute to them.

1.6 The seas around the UK are amongst, if not the, best studied in the world. Knowledge of the ecosystems, habitats and species they contain, their health and trends in their status have been the subject of a number of recent reports [1-3] and repeating that information here would serve little purpose. Rather the report draws on a number of these studies and considers the implications of the observed status and trends for the health of the systems’ functioning and the risk to the ‘goods and services’ they provide (Chapter 3). The impacts of a wide range of human activities on the various components of the marine ecosystem have been described extensively over the last 40 years. This report does not seek to repeat this catalogue of potential impacts, but rather use this knowledge to predict the risk to the systems’ functioning.

1.7 While the waters around the UK may be well studied, the general conclusion from Charting Progress (2005) which reviewed the state of the UK seas, found that data, particularly for offshore areas, was sparse or non- existent, and data on long-term or broad spatial scales was rare, resulting in inconclusive evidence for change [1]. Also, whilst ecologists first began considering ecosystem ecology in the late 1960s, it is only with recent advances in field measuring techniques and advanced computing power (to allow complex simulation modelling) that it has begun to yield to scientific enquiry. At present, grasslands are the most studied environment (they have an economic value, are accessible and easy to experiment with). Yet, even for these comparatively well studied systems, there is still considerable uncertainty as to the nature of relationships such as between productivity and biological diversity. There is even less confidence in the nature of such relationships for marine systems.

Aims

1.8 The specific aim of this report was to provide evidence to support the development of policies to improve the conservation of marine biodiversity by detailing:

• the importance of marine biodiversity and the current status and trends in the UK’s marine biodiversity; and • any decline, loss or deterioration and the likely consequences for the delivery of ecosystem goods and services.

1.9 The report uses a series of examples to do this, as a complete review of all aspects of marine biodiversity in the whole of the UK’s seas would run to many volumes and is unnecessary in considering the key question as to whether new policy or instruments are required to protect the functioning of the marine ecosystems around the UK. This report does not consider intertidal regions as a range of management measures have already been developed for these areas.

Approach adopted

1.10 A pragmatic approach was adopted to complete this review and the subsequent assessment. There is a continually growing body of ecological theory, models and experimental data available. Given that the UK seas are well studied, the data available were used along with the understanding of system functioning that is emerging, to draw some, tentative, conclusions about the risk human activities pose to ecosystem goods and services in UK waters. Both the nature of the data available and the under-pinning science influence the confidence in the conclusions drawn (Chapter 4). As the conclusions are tentative, any management measures developed in consequence should be both ‘precautionary’ and form part of an ‘adaptive management scheme’. Management should be reviewed regularly and adjusted based on new scientific understanding and evidence gathered from monitoring the management measures’ ability to deliver its objectives.

Report Structure

1.11 The report is structured into five chapters plus two appendices. Chapter 2 considers the species, habitats and ecosystem processes that are important for the supply of goods and services in the UK marine environment and provides an assessment of their importance in a European and global context. Chapter 3 summarises the evidence for changes in the status of the ecological component delivering the key ‘goods and services’, while Chapter 4 makes an assessment of the potential risks associated with these changes. Chapter 5 presents a discussion and concluding remarks on the projects findings. The appendices provides a summary of available evidence on the status and trends in the organisms delivering the ecological goods and services and resulting changes to ecological functions.

Chapter 2 - Species, habitats and ecosystem processes important for the supply of ecosystem goods and services to the UK

2.1 The supply of ecosystem goods and services

2.1 An ecosystem is typically defined as “a biological community of interacting organisms and their physical environment.” (Oxford English Dictionary online – www.askoxford.com), thus the key elements are the biological organisms, the physical (and chemical) environment and the interactions between these components. 2.2 The ecosystem can be seen to deliver a variety of goods (e.g. food resources) and services (e.g. waste assimilation and treatment). It must be remembered that these are consequences of the activities of the organisms present, their life processes and their interactions with the physical, chemical and biological systems in which they live. Ecosystems are abstract, human imposed, units and do not exist to, nor strive to, deliver any particular suite of goods and services. Therefore the range of ecological goods and services provided by any ecosystem, be it a rock pool or the North Atlantic, is entirely dependent on the species present in the system and their life processes (Table 1 provides a list of goods and services supplied by the UK marine environment). 2.3 In some cases it is possible to measure the ecosystem goods and services directly, but in most cases it is not, and reliance must be placed on predictive tools, such as modelling, which are based on measurements of organism abundance and process rates. For both ecological and practical reasons, consideration of the delivery of ecological functions must, therefore, proceed from an understanding of the identities and roles of the organisms comprising the biological assemblage [4]. 2.4 It should be noted that many of the key ecosystem processes, including much of the primary production of food, the breakdown of pollutants, and the cycling of nutrients, are carried out by microbes. There is very limited knowledge of the ecology of the microbial system in the marine environment (or on land). Genetic markers for key enzymes tell us something about the availability of, for example, nutrient processing capacity but not in what organisms the enzymes reside or how the organisms might respond to changes in other parts of the ecosystem. However, while microbes are the actual ‘doers’ they are strongly influenced by the actions of the larger organisms in the system where more understanding does exist [5-7]. 2.5 Many natural ecosystems have an inherent ability to show recovery following disturbance. This is only possible for impacts that are below a certain threshold. Disturbances that exceed that threshold force the system into a new configuration. The ability to recover is a valuable property. It means systems can tolerate the impacts of human activities, up to a certain point, without an alteration to the system’s dynamics and the delivery of ecosystem processes. The ability of a particular ecosystem component to resist an

impacting activity (resistance) and its ability to subsequently recover (resilience) varies and is dependent on the biology of the species present.

2.2 Assigning importance to ecosystem components

2.6 For the purposes of this report, the ecosystem was partitioned into six components:

• plankton (primarily microscopic organisms, but also including larger organisms that float in the water e.g. jellyfish and comb jellies); • benthos (organisms which live on or in the sea floor); • fish; • marine reptiles and mammals (e.g. sea turtles, dolphins, seals); • seabirds; and • seafloor habitats.

2.7 This approach has previously been used both to ease consultation with stakeholders and to make the modelling of ecosystem responses to management more tractable [8]. It has also formed the basis of recent ICES/OSPAR work to develop integrated metrics of system health [9, 10]. 2.8 Criteria were developed and used to assess the importance of individual habitats and species. The principle criteria were based on economic or societal importance. Species exploited commercially (either directly by harvesting, or indirectly, through ecotourism) were included. 2.9 Identifying species and habitats important to society was based on their inclusion in international legislation and agreements. The identification of additional important habitat types was based on an assessment of their functional importance. This was assumed to be correlated with their extent which were estimated from maps of marine landscapes (Figure 1). [This assumption is unlikely to be supported for any given function e.g. muddy habitats are more important for nutrient regeneration functions than reefs, but it is a reasonable to assume that the larger and therefore more common habitats will support a high proportion of the total functioning than the smaller ones, and will therefore be of greater functional importance at the scale of UK waters]. Details of the criteria and their application are given in Appendix 1.

2.3 Assigning Importance to ecosystem goods and services

2.3.1 What are ecological functions? 2.10 Ecosystem functioning refers to the processes and activities which keep a system working [11] and has numerous definitions including: ‘the activities, processes or properties of ecosystems that are influenced by its biota’ 12].

2.11 Other definitions include nutrient recycling [13, 14], the flow of energy

and materials through the biotic (living)/abiotic (non-living) components of ecosystems [15], a combination of ecosystem processes and ecosystem stability [16] and the sum total of these processes [17]. 2.12 The environment has different types of value to humans (i.e. economic use and non-use) which have been categorised by various authors to make economic value estimates (see Table 1 for categories). Not all of these values are relevant in the marine environment and the number of categories considered in this report has been further reduced from those used elsewhere to bring together functions that are delivered by the same ecological process to reduce duplication and to reflect gaps in knowledge. Table 1 shows how the limited number of categories were used and how they were mapped to other valuation categories schemes.

Source: unpublished draft UK marine landscapes courtesy of the JNCC [18]

Figure 1. The distribution of marine landscape features in UK seas.

2.13 For the purposes of this report, the provision of ecological goods and services are considered under 5 categories: • atmospheric gas assimilation and climate regulation; • nutrient recycling; • waste assimilation capacity; • habitat functions; • food provision; and • biodiversity for society (i.e. recreation: angling, bird watching, boating, coastal visits and diving, existence and cultural values)

2.14 These five categories therefore cover the key ecological functions delivered by the UK marine ecosystem (Table 1).

Table 1. Categories of ecosystem goods and services as defined by Costanza et al. (1997) for their global environmental valuation, and by Beaumont and Tinch (2003) for their analysis for the UK seafloor and their relationship to the groupings used in this report2. Costanza et al. [19] Beaumont and Tinch [20] Frid and Paramor ecosystem service ecosystem service ecosystem service categories categories categories

1. Gas regulation 6. Gas and climate Gas and climate regulation regulation 2. Climate regulation

3. Disturbance 9. Disturbance prevention Table body text regulation and alleviation A

8. Nutrient cycling 5. Nutrient cycling Nutrient cycling

9. Waste treatment 7. Bioremediation of waste Waste treatment

11. Biological control

12. Refugia B 8. Biologically mediated Habitat functions habitat

13. Food 1. Food provision Food and material provision C 14. Raw materials 14. Raw materials

15. Genetic resources

16. Recreation 3. Leisure and recreation

10. Culture and heritage

11. Cognitive values

12. Option use value Biodiversity in support 17. Cultural D 13. Non Use values – of societal values Bequest and Existence

4. Resiliance and resistance A Relates primarily to the flood prevention role of intertidal habitats which are not considered in this report B The supporting text in Costanza et al. (1997) [19] makes it clear that this function is provided by the habitat C Provision of raw materials other than foods are small in the UK and the issues are not different from those surrounding food provision. D While this issues are distinct economic categories, the relationship to biological diversity are the same so that they are considered together.

2 Constanza et al. (1997) considered categories 4-7 and 10 (water regulation, water supply, erosion control and sediment retention, soil formation, pollin ation) as not being relevant to marine ecosystems

2.3.2 Atmospheric gas assimilation and climate regulation 2.15 The oceans play a major role in global climate regulation both because of their massive heat capacity, which buffers variations in temperature, and because ocean currents move heat around the globe. The temperate nature of the UK climate compared to that of similar latitudes in the north east USA for example, attest to the warming effects of the ‘Gulf Stream’. 2.16 The oceans also play a role in atmospheric processes through the chemical exchanges that occur across the air-sea interface. The atmosphere is the major source of some contaminants which enter the oceans, but the oceans also recharge the atmosphere with oxygen and absorb carbon dioxide. While some of this is a purely physical-chemical process, most is mediated by biological systems. For example the flux of oxygen to the atmosphere is derived from marine plant photosynthesis. However, some of the chemicals absorbed into the ocean are sequestered into deep sea sediments and so are effectively removed from the living, dynamic, part of the global system. Planktonic organisms, such as coccolithophorids and radiolarians, use the dissolved carbon dioxide to produce shells of calcium carbonate. When the organisms die, their shells, being large and heavy, rapidly sink to the seafloor taking the carbonate (carbon dioxide) with them. Some marine plants also liberate gases which are important in stimulating cloud formation. The cloud cover of the planet is important because it reflects some incoming radiation, traps some heat (and so buffers the variation at the planet surface) and alters patterns of rainfall. Without the living marine ecosystem, the Earth’s atmospheric systems would be less hospitable to life on land.

2.3.3 Nutrient recycling 2.17 Nutrient availability strongly affects productivity in the marine environment [21]. Nutrient concentrations in the water column follow a strong seasonal cycle with blooms of phytoplankton (microscopic plants in the water column) in the spring and autumn. These occur as the surface and deep waters are mixed during the winter storms, bringing nutrients from the deeper areas up to the surface. 2.18 The ecosystem of the continental shelf typically receives half the nutrients it requires for primary production from the sediment [22]. These nutrients are derived from the dead material which accumulates on the sea floor [23]. This organic material is decomposed by bacteria which releases the nutrients back into the water column through chemical diffusion processes which may be enhanced by sediment irrigation activities performed by benthic communities [24]. The chemical relationship between the water column and seafloor is tightly coupled [6, 25, 26].

2.3.4 Capacity for waste assimilation 2.19 The marine environment represents an important sink for waste material discharged directly into the sea via outfalls (point source discharges) and via rivers/estuaries and the atmosphere (diffuse source discharges).

These wastes may be assimilated by living organisms [27-29] or may become locked in the sediment [30-33]. 2.20 Non-biodegradable substances, such as heavy metals, and some synthetic substances, such as pesticides and PCBs, may be dispersed by water movement and dilution [34, 35], or may become concentrated in living organisms. This can lead to a magnification of these substances up the food chain, causing health concerns for top predators including man [36-39]. 2.21 Biodegradable wastes, such as food wastes and the organic components of sewage, in addition to being dispersed [40], are also subject to breakdown and ultimately decomposed to carbon dioxide and inorganic nutrients.

2.3.5 Habitat functioning 2.22 Habitats provide the ‘living space’ required by organisms. They provide sites for feeding, breeding, sheltering from predators and natural disturbances and thus are a pre-requisite for the provision of many other goods and services. 2.23 Most, but not all, definitions of habitat include both the abiotic and biotic factors that characterise the location. These factors may include physical structures such as sediments, reefs and biological structures. The latter may include worm tubes, coral reefs and the tentacles of jellyfish.

2.24 The availability of the correct ‘habitat’ is therefore a requirement for an organism to survive, grow and reproduce. This critical role is emphasised in the USA by the provisions of the Magnuson-Stevens Fishery Conservation and Management Act (1996) that requires regional fisheries councils ensure effective protection of ‘essential fish habitat’ (e.g. the nursery and feeding habitats of commercial fish species) as part of their commitment to ensuring sustainable fisheries.

2.25 The EC Habitats Directive (1992) [41] requires Member States to provide protection for a limited number of marine habitat types. The habitats types were selected primarily for their societal value rather than to ensure delivery of key ecosystem functions.

2.3.6 Food provision 2.26 The marine environment is a readily available source of food for human consumption. In 2004, the UK fleet landed 654,000 tonnes of sea fish with a total value of £513 million, and supported 11,559 fishermen [42].

2.27 Fisheries exploit a diverse range of species including: • bottom feeding shellfish such as whelks and Nephrops (scampi or langoustine); • shellfish that filter their microscopic food from the water, such as mussels, cockles and scallops;

• fish such as plaice, sole, cod, haddock and skate, that feed on bottom dwelling worms, crabs, sandhoppers and clams; and • fish that feed on other fish and other swimming and floating organisms in the water body (herring, mackerel). 2.28 These fisheries all provide food directly for human consumption. Smaller fish such as sandeels, Norway pout and blue whiting are harvested and converted into fish meal which is used to make animal feeds, including feeds for use in fish farms. Therefore farmed salmon, trout and sea bass derive part of their nutrition from the food provision service provided by the UK seas. 2.29 In addition to the harvesting of sea fisheries resources, further revenue and employment is also created through the fish processing industry, retail sales, and exports, with fish processing employing approximately 18,180 people, and 1,300 fishmongers. Many of these jobs are concentrated in remote communities. 2.30 Landings by the UK fleet into the UK have remained around 460,000 tonnes over the last five years. Demersal species (fish that feed on organisms in/on the sea floor) represents 34 per cent of total landings in terms of quantity and 41 per cent in terms of value. Pelagic species (fish that feed on organisms in the water column) account for 39 per cent of landings by quantity but only 16 per cent by value. Shellfish account for 27 per cent of landings by quantity and 43 per cent by value (Table 2).

Table 2. The quantity & value of UK fish and shellfish landings 2000-2004 Quantity (‘000 tonnes) Value (£ million) 2000 2001 2002 2003 2004 2000 2001 2002 2003 2004 Demersal 301.0 270.3 242.5 202.7 231.1 302.3 281.1 257.2 219.9 223.5 Pelagic 311.8 323.7 305.3 292.9 290.9 78.5 114.2 114.4 114.5 105.8 Shellfish 135.4 143.8 137.6 144.0 131.7 169.5 179.1 174.0 193.9 183.7 Total 748.1 737.8 685.5 639.7 653.7 550.3 574.4 545.6 528.3 513.0 Fish (Source: United Kingdom Sea Fisheries Statistics 2004 [42])

2.3.7 Societal value of biodiversity – recreation, angling, boating, bird watching, coastal visits and diving, existence and cultural values 2.31 Recreation has been one of the fastest growing economic sectors in the UK in the last 50 years [43, 44]. Much of the marine and coastal recreation is centred on wildlife and scenery, but the level of dependency varies. Ecotourism activities are usually highly dependent on one or a few species, typically cetaceans (whales and dolphins), birds and/or seals. Recreational sea anglers tend to target a limited number of fish species. Many other sectors concentrate, but not exclusively, their activities in areas which are perceived to be ‘scenic’ or natural, such as SCUBA diving, coastal visits and recreational cruising/sailing. Generally, coastal visits, such as beach use, do not depend on the presence of natural biological systems, but users would be perturbed by some signs of mis-functioning systems, e.g. harmful algal

blooms, or accumulating wastes. 2.32 A recent estimate of the total net value of marine leisure and recreation in the UK was £11.77 billion [45]. This value included income from bird, cetacean and seal watching, aesthetic value, and the indirect value of tourism associated with commercial fishing activity. The importance of these activities, measured as the numbers involved and their commitment to the activity, is shown in Table 3. 2.33 In addition to direct recreational interaction with marine nature, most members of the UK community when questioned, will express a desire/commitment to preserving the natural world.

Table 3. Recreational participation and club membership levels Activity Membership of Estimated % users who governing body popularity have membership 52,247 members Approx. Sub Aqua (British Sub-Aqua Club) 83% 120,000 51,700 members

(PADI) 221,699(National Federation of Anglers) Angling 2,500,000 35,000(National 0.1%

Federation of Sea Anglers) 1 million (Royal Society 2 million Ornithology/ for the Protection of 50%

Birdwatching Birds) (Source: UKCEED [46])

2.4 The importance of the UK’s seas in a global and European context

2.34 The UK seas form a major part, around 7.6%, of the European Seas and the economic benefits of the marine environment to Europe are, to a large extent, dependent on the health and status of the seas of the Ireland, UK and Spain. Thus, delivery of clean, healthy and sustainable European marine waters is dependent, in large part, on activities in the UK sector [47]. 2.35 The UK’s marine area covers 867,000 sq km (335,000 sq miles) which is more than three times the UK land area, or to put it another way, over three- quarters of the UK’s total area is sea. 2.34 The scale of marine dependent activities is significant and includes: • the UK fish and shellfish catching industry which lands over £540 million in catches each year, resulting in between £800–1200 million of economic activity in the UK [48]; • UK recreational anglers spend around £1 billion per year on their sport [49];

• Offshore oil, gas and aggregate extraction is worth over £20 billion per year (http://www.og.dti.gov.uk/information/bb_updates/appendices/Appendix 7.htm); and • Off-shore wind-power installations. With a UK target of 10% of energy generation from renewable sources by 2010, considerable growth in the offshore renewables sector is expected and this will be stimulated by Government investment, via the Climate Change Levy, of over £1 billion per year by 2010 (http://www.dti.gov.uk/energy/sources/renewables/policy/offshore/page 22500.html). 2.36 In addition to these, the marine environment potentially provides an important resource for bio-prospecting although this has yet to be fully explored. 2.37 In addition to these direct uses of the marine environment, the seas provide many indirect benefits: • they are a major reservoir of biological diversity with over 44,000 species[50] recorded;

• they are a major store of the greenhouse gas carbon dioxide (CO2) and assist in regulating the Earth’s climate; and • organisms in the sea play a vital role in nutrient recycling, returning nitrogen, phosphorus and sulphur to the biologically active part of the global ecosystem. 2.38 Turnover and value added by the marine sector is shown in Table 4. Between1999-2000, the contribution of marine-related activities to the UK economy was estimated to be £39bn, or 4.9% of Gross Domestic Product (GDP). In 1994-95, the estimated contribution was £27.8bn, or 4.8% of GDP. Excluding tourism, the 1999-2000 figure is 3.4% of GDP. This further confirms the importance of marine activities to the UK economy [45].

Table 4. Turnover and ‘Value Added’ by the marine sector in the UK economy (Re-valued to 1999 prices, all £ million) 1994-5 1999-2000 Sector (£ million) (£ million) Turnover Value Added Turnover Value Added Oil and Gas 15295 12310 20597 14810 Leisure 10129 6859 19290 11770 Defence 6762 2703 6660 2531 Business Services 6417 1099 4535 1080 Shipping 5007 2317 5200 2400 Ship building 4002 1875 3172 1574 Equipment 3565 1438 2326 1358 Fisheries 2392 822 2447 825 Environment 1380 460 1050 435 Ports 1311 918 1690 1183 Construction 826 231 500 190 Research 645 309 609 292 Telecommunications 460 230 500 190 Safety 336 138 316 129 Crossings 178 100 155 87 Aggregates 168 87 131 69 Education 54 28 49 25 Total 58927 31923 69227 38948 (Source: Pugh and Skinner, 2002 [45]) 2.39 The total marine Exclusive Economic Zone (EEZ) claimed by the EU extends to 11,447,075km2. The three largest national contributors are Ireland (890,688km2, 7.8%), the UK (867,000km2; 7.6%) and Spain (683236 km2, 6.0%) (http://earthtrends.wri.org/country_profiles/index.php?theme=1&rcode=2). Portugal is the only other EU nation with oceanic and coastal seas. Therefore, the UK has both a significant proportion of the total European seas and is responsible for a large part of the oceanic component of the European EEZ. So while it is impossible at this time to partition the goods and services provided by the European seas to any particular area there is a good basis for considering the UK’s marine waters to be important in the European context. 2.40 The global ecosystem has been estimated to provide around US$33 x 1012 to the global economy of which some US$21659 x 109 is contributed by aquatic systems [19]. The majority of this is derived from coastal systems which deliver 16 times more goods and services than oceanic areas hectare for hectare.

Chapter 3 - Evidence of status and trends in UK marine biodiversity

3.1 A lack of detailed information makes it difficult to draw robust conclusions about the health of the marine environment [1, 51]. For some organisms, good data at a limited number of locations exists (e.g. seabirds and seals at their breeding colonies), whilst for other groups, only data that allow trends over time to be established exist, but for only a part of the system (e.g. CPR [52]). Available data and trends were summarised in ‘Charting Progress’ [1]. 3.2 A limited number of case studies covering important species and habitats, outlining known information on current trends and status, and how these in turn affect delivery of ecological functions have been prepared (Appendix 2). The case studies have been selected to provide illustrations of how important species (and groups of species), habitats and goods and services have changed in recent times. For most species/groups of organisms, habitats and the resultant goods and services, there is a lack of the data necessary to make robust assessments for the entire UK marine area.

3.1 Important Ecosystem goods and services 3.1.1 Atmospheric gas assimilation and climate regulation 3.3 There are no direct measures of gas fluxes into and out of the UK seas, and the large scale data provided by satellite and other remote sensing operations provide only information on surface abundance of plant pigments. Given that the rate of gas use/production and other biogeochemical processes often vary between species of plant, it is impossible to make detailed inferences about any changes in status of these ecological services.

3.4 Although there are no data that provide direct estimates of the flux of gases in and out of the UK seas, it may be possible to calculate some of the important elements of the flux using oceanic models. For example, the climatically active gas dimethyl sulphide (DMS) is produced from gases released by planktonic algae such as Emiliana huxleyi. Blooms of Emiliana huxleyi, can be documented from satellite imagery. Thus it is possible to calculate the production of DMS. Estimates suggest that Emiliana huxleyi blooms might be important regionally, but play only a minor role in the global regulation of climate [53]. There is some indication that the centre of Emiliana huxleyi activity is moving northwards (see Appendix 2).

3.1.2 Nutrient Recycling 3.5 Nutrient concentrations in the water column follow a strong season cycle. The annual spring phytoplankton bloom is linked to the mixing of the water column during the winter storms. This mixing brings nutrients from the deeper waters up to the illuminated surface waters which allows

photosynthesis to occur. Autumn blooms occur when the stable water column produced in the summer breaks down and nutrients are brought up to the surface. This bloom is curtailed by the diminishing levels of light as autumn advances. There is some evidence that the timings of the bloom is being influenced by climate change [54]. This will impact food web interactions but it is unclear how these changes will affect nutrient recycling. Evidence from the continuous plankton recorder (CPR) shows that within the phytoplankton, diatoms (microscopic plants that secrete a silicon ‘shell’) are now less abundant, whilst dinoflagellates (small rapidly growing plant cells) are becoming more common. As diatoms take up silica, and dinoflagellates do not, this certainly means an alteration in the cycling of silica. Dinoflagellates and diatoms also use different amounts of other plant nutrients, particularly nitrate and phosphate. Thus we can conclude that the observed changes in the size, timing and composition of phytoplankton blooms will have resulted in altered patterns of nutrient uptake and so altered the cycles. A lack of detailed historic data however means that we cannot measure these changes directly. 3.6 Although there is information on the biota which contribute to nutrient recycling (e.g. burrowing worms), and some measure of their processing rates, there are very few studies which have measured the direct effects of human activities on nutrient recycling [55, 56]. The effect of long-term changes in the benthos on nutrient recycling processes is unknown. 3.7 Trimmer et al., (2005) [56] showed that fishing had no impact on oxygen uptake, denitrification or nutrient exchange in the southern North Sea. In the long-term, chemical processes in the upper layers of sediment appeared unaffected by trawling. This may be because any changes in nutrient recycling which are likely to have occurred as a result of fishing had already happened by the time studies began.

3.1.3 Waste assimilation capacity 3.8 The seas have a finite capacity to absorb human-derived wastes without showing detrimental changes. The limit is set by the rate of removal (dilution) and the breakdown/assimilation capacity. For organic wastes and nutrients, the key limit is usually determined by biological processes. For other wastes, it is the dilution capacity [57]. There are many well documented cases of the adverse impacts arising from excessive waste inputs. However, these tend to be limited to near the region of input. It follows logically that reductions in the size of inputs and the number of sites for waste disposal will reduce these adverse effects and mean that the system will have a great capacity to function naturally. 3.1.3.1 Hazardous wastes 3.9 Large reductions in the input of most hazardous wastes to the marine environment have occurred over recent decades [1]. Total inputs via rivers and directly of mercury (Hg), cadmium (Cd), copper (Cu), lead (Pb), Zinc (Zn) and the organic contaminant known as γ-HCH to coastal waters have been reduced by 20%-70% since 1990, and atmospheric emissions of the same chemicals have been reduced by 50%-95% since 1990. However,

concentrations of Hg, Cd, Cu, Pb and Zn in both water and sediments are elevated. Highest concentrations of hazardous substances in biota were found in industrialised estuaries and adjacent areas with a known history of contaminant inputs. High concentrations of Cd were also found in fish livers from the offshore Dogger Bank site. 3.10 Discharges of radionuclides from Sellafield have decreased significantly since the 1970s, as a result of various measures. In most cases, current discharges are at least 100 times lower than peak discharges in the 1970s. 3.11 The National Marine Monitoring Programme (1998) report states that fisheries and wildlife do not appear to be in serious decline due to contaminant effects, and the concentrations of many contaminants are apparently decreasing [58]. However trace or microcontaminants are still causing demonstrable polluting effects in areas where certain marine discharges are poorly diluted, or where this is a legacy of persistent pollutants in fine-grained sedimentary sinks [59]. 3.12 Overall, the great advances made in recent decades to reduce polluting inputs will mean that the systems waste assimilation capacity is healthier now than in the recent past. 3.1.3.2 Sewage disposal 3.13 Sewage inputs to the sea have decreased dramatically since the 1980s following the implementation of the Bathing Waters [60], Shellfish [61] and Urban Waste Water [62] Directives. These have resulted in marked improvements in UK coastal waters [59]. Sewage inputs (including effluent from treatment works) and fertiliser run off, potentially contribute to eutrophication (the stimulation of plant growth above natural levels, often leading to undesirable effects). 3.1.3.3 Nutrient input 3.14 Direct inputs of nitrogen and phosphorus in the UK have been reduced by 35% and 50%, respectively since 1990 [1]. However, there is no evidence of reductions in the quantities entering coastal waters from rivers which mainly arise as diffuse inputs of nutrients from land run-off. The input from diffuse sources varies with rainfall and river flow rates and varies in the different regions. Although the coastal waters of southern, eastern and north-western England and the inner Bristol Channel are enriched with nitrogen and phosphorus, the correlation with nutrient input is weak [1]. The reduced nutrient inputs are not reflected in a detectable reduction in the winter nutrient concentration in the sea. This reflects the importance of the ocean as a source of nutrients to UK coastal and offshore waters. 3.1.3.4 Hydrocarbons 3.15 Inputs of oil from land based sources, including refineries and offshore operations are tightly regulated and the total input from offshore sources is fairly constant [1]. Spillage of oil from accidents offshore or from tankers or other maritime accidents is by definition irregular and impacts are localised and transient.

3.1.3.5 Dredged material 3.16 Ports, harbours and shipping channels can silt up with sediment. Approximately 25-40 million wet tonnes of dredged material is removed annually from access channels, ports, marinas and harbours and deposited in ~150 licensed disposal sites. Since 1992, there has been a slight increase in the overall quantity of dredged material deposited at sea each year. More than 60% of all dredged material is deposited in the southern North Sea and the Irish Sea. Monitoring has demonstrated that impacts tend to be confined within the boundaries of the disposal sites, and impacts are site specific [63]. 3.1.3.6 Overview 3.17 The levels of material disposed of in coastal seas and estuaries in the recent past will have impacted on their ability to deliver key ecological goods and services. Recent years have seen major reductions in the levels of discharges and investment in onshore treatment. This will have reduced the degree to which the system is compromised and so has increased the ability to absorb occasional insults such as accidental spillages. However, there remain a number of localised areas, particularly some estuaries, where historical inputs still cause measurable declines in the health of the marine ecosystem.

3.1.4 Habitat functions 3.18 No definitive map of the actual distribution of UK seafloor habitats currently exists making it impossible to assess whether the area of certain habitat types has changed and what they have been replaced with. In some cases we do have evidence of habitat loss (e.g. cold water coral reefs, maerl beds, mussel (blue and horse) and oyster beds) and can infer the loss of the habitat provision and other functions associated with them (see Appendix 2 for details). 3.19 One patch of a habitat, for example, muddy sand, is also not identical to another patch of muddy sand in terms of the biological assemblage it supports and the ecological functions it delivers. This variation within a habitat is sometimes referred to as ‘habitat quality’. There is evidence that in some areas habitat quality has been impacted, for example at dredge spoil disposal sites, and yet the impacted seabed may still be characterised as the same habitat as the surrounding areas, despite its lower quality. Any change in species composition implies that the area might be delivering different ecological functions from the natural situation [4]. 3.1.5 Food provision 3.20 Over the past decade, the status of stocks of some key demersal (bottom living) fish species has deteriorated [47]. In contrast, the state of pelagic species (those that live in the water column), such as herring, has improved. In the North Sea, four of the eight main demersal stocks are harvested unsustainably or are at risk of being harvested unsustainably. The cod stock remains at historically low levels and is subject to emergency management measures and a recovery plan from 2005. In contrast, herring stocks have increased and the quotas for Nephrops (scampi) in the North Sea

have been increased this year suggesting that they are exploited sustainably (T.L. Catchpole (CEFAS), pers. comm.). 3.21 Over the past decade, Irish Sea cod and whiting stocks have declined raising concerns over possible stock collapse. Most demersal stocks in the southwest approaches are harvested outside of precautionary limits. The northern hake stock is the subject of a management recovery plan introduced in 2004 that includes a lower Total Allowable Catch and technical measures (mesh size restrictions). Haddock and Nephrops in the west of Scotland are harvested sustainably but the status of many of the other demersal species are either uncertain or considered to be at low historical levels. 3.22 Many factors can cause changes in the abundance and distribution of fishes, including natural variation, biological interactions and human activities. Activities that are known to affect the structure and diversity of fish communities include fishing, changes to habitat quality caused by, for example, pollution, eutrophication and habitat destruction, and the introduction of non-native species. Determining the relative impacts of these various factors is difficult however, and while some studies have shown a correlation between environmental variables and biological components, there are few cases that prove causal relationships. 3.23 Commercial exploitation of fish also has impacts on the wider marine environment. These impacts include those on the abundance, size and genetic make-up of target species, on seabed habitats and non-target animals such as marine mammals, fish and benthic fauna that are also caught during fishing operations, on the genetic diversity of both species and populations, and on the food web itself. Fishing affects non-target species caught as bycatch, and has caused reductions in large bodied and vulnerable species such as skates and rays. Monitoring programmes to determine the quantity and composition of discarded catches are in place in many UK fisheries. Many of the larger target and by-catch species in the North Sea and Irish Sea are now reduced to <10% of their expected abundance without fishing, and the mean weight of fish has declined. 3.24 Therefore the trend in the provision of food from the sea is one of overall decline. This in turn has driven the fishing industry to seek new species, exploit new habitats (e.g. deep water) and fish harder to maintain catches. These changes will have negatively impacted on the supporting ecosystem compromising its ability to deliver goods and services and to support the fisheries.

3.1.6 Biodiversity for Recreation, existence and cultural values 3.25 No direct assessments of the levels of biodiversity used for recreation exists. Data on biodiversity are collected from national monitoring sites for impact management purposes and often show declines due to human activity. Recreational activities are not universal or uniform in the marine environment and tend to avoid impacted locations as they are less desirable to the public. The available data suggest that there have been significant increases in recreational sea angling, boating, sport diving, coastal visits and eco-tourism in the last decade [64]. This implies that biodiversity levels, at least in these areas, is sufficient to meet the needs of the existing users. 3.26 Data for fish catches and comments from the National Federation of Sea Anglers [65] suggest concerns over the numbers and diversity of fish available for anglers. Sea bird and marine mammal populations are generally increasing but in many cases should be regarded as fragile. Many recreational activities potentially damage the marine environment – angling, cruising and diving boats for example may damage fragile seabed habitats when anchoring, visitors to the shore may impact the system through trampling, litter and disturbance. Management therefore has to balance the need to protect the environment with the positive benefits of a larger proportion of the population engaging in nature-based recreation [66].

Chapter 4 - Assessment of risk to the supply of important goods and services

4.1 Chapter 4 considers, for each of the five ecosystem goods and services categories being considered, the risk of collapse. This includes an assessment of the evidence of declines/deteriorations in the ecosystem components that deliver the ‘goods and services’ and the level of ‘redundancy’ in the system, i.e. if a component fails, is there another that would still be able to deliver the same goods/services? 4.2 The assessment draws on the analysis presented in Chapter 3 and the detailed material contained in Appendices 1 and 2. It is constrained by the same limitations; a lack of available data for all components covering the necessary areas and timescales. However, logic would suggest that a comprehensive assessment is not necessarily required, because if there is a risk of failure in any part of the system, then it needs to be addressed. 4.3 The quality and diversity of the information used for this assessment implies a qualitative rather than a quantitative assessment. The quality of evidence and the risks are assessed using a standard terminology to aid comparisons. These are defined in Table 5. 4.4 Given the nature of the data and the still immature nature of the science in the area of biodiversity and ecological function, all conclusions drawn are tentative. Nor should it be assumed that stopping a damaging activity will necessarily cause the system to revert to its pre-impact state.

4.1 Timescales for changes

4.5 Given the high degree of natural spatial and temporal variability in marine ecosystems, long-term monitoring at relatively high intensities is required in order to understand variability patterns and to be able to comment meaningfully on their dynamics. It is also the case that many marine systems show a high degree of resilience, allowing recovery from disturbances (see Box 1). 4.6 Extreme perturbations can lead to shifts in the dynamics of the system, so called phase shifts or alternative stable states [67]. One of the clearest examples of such a shift in marine systems has been in the Black Sea following the fishery collapse and subsequent invasion by a non-native species of jellyfish [68].

Box 1: Seabed recovery The seafloor off Northumberland was used for the dumping of ash from a power station. Whilst this was occurring, an area of around 14km2 was essentially without life as, almost everyday, the dumped ash smothered the sea bed. Following the end of waste dumping at sea in 1992, the seabed began a process of recovery and within 9 months all areas had been colonised. A community similar to the background community was established within 3 years [69]. Studies following gravel extraction show considerable variability between sites, but generally periods of rapid improvement are followed by a prolonged phase of further continual improvement. Full recovery may take over 10 years, although if long lived, slow growing, species have been lost then complete recovery may never occur [70-73].

4.7 Both the impact of the introduced species, and recovery rates, highlight that marine systems can undergo very large changes in short time frames. Theory would suggest that in many cases, species diverse systems do not show a gradual steady decline with increasing impact. Rather systems may show little change and then suddenly change dramatically. In the current context this implies that ecological functioning would initially be maintained but could suddenly collapse. Given our limited knowledge of marine system dynamics this argues for a precautionary approach with a high degree of risk avoidance. Monitoring is not likely to detect that the system has reached the threshold until after it has passed it and key ecological functions are no longer available. This interpretation has been placed on the Canadian Grand and Georges Banks cod collapses and the subsequent lack of recovery even after 15 years of complete fisheries closures (J. Rice, DFO, pers. comm.).

Table 5. Definitions of standard terms used to define the quality of the evidence for changes in critical ecosystem components and the associated risk to delivery of ecosystem goods and services Quality of the Evidence Risk None No evidence on Low Existing levels of change, or which to form a continuation of the observed judgement. trend is unlikely to result in failure of the ecosystem to provide the goods/services or there scope for provision to be met from other parts of the ecosystem. Some Evidence of Moderate Existing levels of change, or changes in the continuation of the observed ecosystem trend is likely to result in failure components is of the ecosystem to provide the restricted to a current levels of, or the full range limited spatial of goods/services. There might area, confounded be some scope for provision to with other be partly met from other parts of changes or the ecosystem. largely inferred. Good Clear evidence High Existing levels of change, or from a number of continuation of the observed studies/ areas trend is likely to result in failure that show of the ecosystem to provide the deterioration in goods/services and there is little key ecosystem or no scope for provision to be components. met from other parts of the ecosystem.

4.2 Risk evaluation for atmospheric gas assimilation and climate regulation

4.8 There is good evidence from the Continuous Plankton Recorder of changes in both the level and seasonal pattern of phytoplankton blooms around the UK (Appendix 2). Changes appear to be driven more by climatic variations than nutrient inputs, but elevated nutrients may contribute both to the level of production and alterations in the species composition of blooms. These changes will influence the production of the atmospherically active DMS gas but calculations suggest that changes in Emiliana huxleyi and other algal blooms are unlikely to influence longer term sequestering of CO2 (http://www.noc.soton.ac.uk/soes/staff/tt/eh/biogeochemistry.html). In part, this is due to species replacements occurring, such that the total drawdown of CO2 remains unchanged. This conclusion is tentative and some studies contradict it. Furthermore ecological theory and studies in enclosed bodies, such as freshwater lakes, suggest that it is likely that once a threshold is past, species replacements will no longer compensate for loss. There are no data to allow prediction of this threshold for collapse.

Conclusion

There is GOOD evidence of deterioration in the ecosystem components that support the ecosystem services that regulate the atmosphere and climate. There is a LOW-MODERATE risk that these changes could lead to undesirable consequences for the atmosphere and climate.

4.3 Risk evaluation for nutrient recycling capacity 4.9 Although there is evidence that the organisms associated with nutrient recycling have been affected by human activities over the last century (see Appendix 2), there is little evidence to suggest that the total rate of these processes has been altered. Conclusion

There is SOME evidence of deterioration in the ecosystem components that support the ecosystem services that provide nutrient recycling. There is a LOW risk that these changes could lead to undesirable consequences for the recycling of nutrients.

4.4 Risk evaluation for loss of waste assimilation capacity

4.10 There is good evidence from the Continuous Plankton Recorder of changes in both the level and seasonal pattern of phytoplankton blooms around the UK (Appendix 2). Changes appear to be driven more by climatic variations that nutrient inputs, but elevated nutrients, from agricultural runoff and sewage treatment, probably contribute both to the level of production and altered the species composition of blooms. These changes could lead to altered food web dynamics and hence altered drawdown of nutrients and hence altered waste assimilation capacity for organic wastes.

4.11 Improvements in waste disposal regulation in recent decades has decreased pressure on the systems’ waste assimilation capacity and, except in localised areas, there appears to be low risk of loss of this function if current trends in waste disposal continue.

Conclusion

There is GOOD evidence of deterioration in the ecosystem components that support the ecosystem services that provide waste assimilation. There is a LOW (MODERATE for nutrient containing wastes) risk that these changes could lead to undesirable consequences for ability of the system’s waste assimilation capacity.

4.5 Risk evaluation for habitat functions

4.12 There is good evidence that habitats have been affected by human activities (Appendix 1). Some habitats are very sensitive to disturbance and

may be permanently destroyed by a single impact (e.g. cold water coral reefs), whilst other habitat types may be more tolerant to disturbance (e.g. sands). There is evidence that long-term and high frequency activities, such as fishing, have affected their ability to support ‘natural’ communities and there exists the very real possibility that major, and ecologically important, changes occurred prior to any scientific studies. This is suggested by studies using data from the early twentieth century [74, 75] and the fossil record [76].

4.13 There is good evidence of losses to biogenic habitat types such as seagrass beds [77-79], shellfish reefs (oyster and mussel beds) [80, 81], maerl [82, 83], worm reefs (Sabellaria alveolata) [80, 84] and cold water coral (Lophelia) reefs [85-87] within the last century as a result of human activities. Loss or damage to these habitat types will result in a reduction of the high levels of biological diversity, and the functions these communities provide.

4.14 There is evidence to suggest that damage to some of the more common, and more resilient, habitat types, such as sands and gravels, has resulted following activities such as aggregate extraction. Some studies have observed clear differences in benthic communities for several years after the cessation of dredging [70],[88]. This may affect the natural functioning of the area.

Conclusion

There is GOOD evidence of deterioration in the ecosystem components that support the ecosystem services that provide societal value. There is a HIGH risk that these changes could lead to undesirable consequences for the delivery of habitat functions.

4.6 Risk evaluation for food provision

4.15 There is good evidence of changes in fish populations around the UK (Appendix 2). These cover both fish species targeted by the fisheries but also the non-target members of the fish community [89, 90]. Some of these changes can be attributed to variations/changes in climate and hydrography, although the single greatest influence is fishing. Given the economic value of fisheries [48] and role of fish in the diet of many species of high public interest (sea birds, marine mammals), the decline of the fish component of the ecosystem is likely to have wide ranging negative effects both on food supply and on biodiversity, and particular the components most valued by society. 4.16 In the North Sea alone, eight species of demersal fish consume around 28 million tonnes of benthic food (worms, clams, brittlestars, sea urchins, crabs, shrimps etc.) each year [91]. As fish species vary in their ability to capture different prey, changes in the amount of benthic food, and the composition of the benthic community, may potentially impact on the food resource of these fish. 4.17 There is clear evidence for a series of changes in plankton in UK waters. These include declines in some key taxa (e.g. Calanus finmarchicus),

but also altered levels and patterns of productivity, and changes in species composition (some species are doing better, some worse). Given that plankton are the base of the marine food chains, these changes are potentially highly destabilising. 4.18 The strong link between shelf benthic communities and the productivity of the overlying water means changes in the amount and probably the timing of plankton production will have implications for benthic communities. This will in turn alter the food supply for demersal fish. 4.19 There is some evidence that changes in plankton has effected the growth and survivorship of larval fish and may be contributing to the decline in some fish populations.

Conclusion

There is GOOD evidence of deterioration in the ecosystem components that support the ecosystem services that support food provision. There is a HIGH risk that these changes could lead to further undesirable consequences for the supply of food from the sea.

4.7 Risk evaluation for biodiversity in support of societal values

4.20 Sea birds have a high public profile and are economically important through eco-tourism and recreational use of biological diversity. They are also protected under UK and European law and numerous international conventions. 4.21 Whilst there is good evidence of a decline in the occurrence of many species of seabird when compared with data from previous centuries, there is also clear evidence of recovery in many species following the introduction of protective measures (see Appendix 2). Sea birds fulfil a wide range of ecological roles but do not appear to be the critical group for the delivery of any particular ecosystem service other than biologically diverse and naturally functioning systems. These species tend to be at or near the apex of the food web and their loss represents a truncation of the natural food web. 4.22 Marine mammals and reptiles have a high public profile and are subject to protection under UK and European law and various international conventions. Marine mammals are often the key resource in marine eco- tourism ventures. 4.23 There is good evidence for declines in the occurrence of some marine mammals and reptiles but also evidence of recovery in some groups, such as seals. These species are not the key for the delivery of any ecosystem services other than biologically diverse and naturally functioning systems. These species tend to be at or near the apex of the food web and their loss represents a truncation of the natural food web.

4.24 There is good evidence of changes in fish populations around the UK. These changes cover both fish species targeted by the fisheries and recreational sea anglers, but also the non-target members of the fish community [89, 90]. Some of these changes can be attributed to variations/changes in climate and hydrography. However, the single greatest influence is fishing. Given the economic value of fisheries [48] and role of fish in the diet of many species of high public interest (sea birds, marine mammals), a decline of the fish component of the ecosystem is likely to have wide ranging negative effects both on food supply and on biodiversity, and particular the components most valued by society. 4.25 To date there is clear evidence of negative effects on birds and shellfisheries of increased frequency of blooms of toxic and nuisance algae.

Conclusion

Table 6. Summary of the analysis of the evidence that biological systems that delivery ecological services have been compromised and the risk to the continued delivery of the service Ecological services Quality of evidence Risk to delivery of of a deterioration in ecological service ecosystem providers Gas and climate Good Low-moderate regulation Nutrient cycling Some Low Waste treatment Good Low (Moderate for nutrient containing wastes) Habitat functions Good High Food and material Good High provision Biodiversity in support Good High of societal values

Chapter 5 - Concluding remarks

5.1 This report has sought to use a limited number of examples to highlight the evidence of changes in ecological goods and services derived from the UK’s marine biological diversity (Table 6). Ecological goods and services arise from the actions of marine organisms as they interact with each other and the environment. Different species contribute in different ways and different amounts to the overall delivery of functions by the ecosystem. Changes in the biological diversity of the system at the species or habitat level will result in a change in the delivery of these functions. The UK seas account for 7.6% of the European sea area and the UK has the second largest share of that resource. The UK clearly needs to maintain a healthy sea both to support the 5% of UK Gross Domestic Product delivered by its waters but also as a contribution to the health of the wider European resource. 5.2 At the time of writing this report data availability and quality are variable on the various marine ecosystem components. It is however sufficient to make a representative assessment of the risk to the provision of important goods and services if there is a change to marine biodiversity [1]. Within the constraints of this study it was not possible to review the data for changes in each ecosystem component in each part of the UK and so develop a comprehensive review of all the ecological functions. For some functions it might be possible to derive levels directly (e.g. fish capture, recreational use of the sea) but for many functions levels of provision have to be calculated based on known process rates and biological data. 5.3 Considering the UK marine ecosystem as a series of component parts, it was found that there is good evidence of deleterious change in all of these components. Thus both biodiversity and the ecological functions the marine environment provides are being altered as a result of human activities. The results of ecological models suggest that in many systems increasing levels of impact lead to small changes in the system followed by a sudden collapse. The demise and subsequent lack of rebuilding of Canadian cod stocks is cited as a real world example of such catastrophic phase shifts with sudden onset. Thus observations of impacted systems and modelling lead to the conclusion that regular monitoring of the system may fail to give warning of system failure and this then implies that management needs to be highly precautionary (risk adverse). 5.4 The levels of risk shown in Table 6 are based on current levels of human impacts. While pressures from waste disposal in the marine environment are decreasing, many other potentially damaging activities are set to increase (offshore energy, aggregate extraction, coastal development, maritime transport). As with all developments, the use of active, innovative, management measures early in the development process could see the actual impacts largely or wholly mitigated. However, a ‘business as usual’/continuation of current policies in the face of growing use levels will see further degradation of the UK’s marine biological resources and the goods and services they provide. The key is effective management and given the inherent complexity of the system and our current state of knowledge, a

precautionary and adaptive management scheme is required. 5.5 The highest risk of a failure in system functioning would result from changes in the microscopic organisms that live in the water, the plankton, and the organisms inhabiting the sea floor (and deterioration of the habitats on which they depend). These groups provide the food resource for all other components but also deliver key services through waste treatment and assimilation, nutrient cycling and atmospheric gas regulation. 5.6 A diverse range of recreational activities, of considerable economic value (£11.7 billion, Beaumont et al. unpublished) are dependent on the higher trophic levels, so while loss of these groups may not greatly impact delivery of most ecosystem functions they would compromise some of the economic benefits gained from the UK’s seas. 5.7 Human activities which influence large-scale patterns will tend to have the greatest effects. In particular, anthropogenic climate change (increasing temperatures, increased storminess, acidification of seawater) are likely to have effects far beyond those resulting from localised disturbances such as fisheries, aggregate extraction and waste disposal. At present limitations in data, scientific knowledge and the lack of suitable tools (models) hinders our ability to fully understand the consequences of our actions. Greater attention to monitoring ecosystem health, more investment in the development of the science and more appropriate models will increase the ability to predict the consequences human activities and so management them in a sustainable manner.

Acknowledgements Nicky Beaumont, Mel Austin and colleagues and Plymouth Marine Laboratory for useful discussions and access to work in progress. Julie Bremner, Jake Rice, Stuart Rogers and Heidi Tillin for comments and fruitful exchanges. The report was considerably improved as result of comments from the external reviewer, Angela Moffat, Jo Myers and Dominic Whitmee.

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Appendix 1

Species of importance

Plankton Plankton are the, mainly, microscopic organisms that drift in the water. They have a high ecological importance due to their importance in the diets of fish, invertebrates and cetaceans [92-96]. Further up the food chain, planktivorous fish, such as sandeels, herring and blue whiting, are important prey to many protected bird species [97-99] and commercial fish species [100, 101]. Phytoplankton (algal plankton) also affect the climate through their influence on atmospheric carbon dioxide (CO2) and dimethyl sulphide (DMS) concentrations [102]. Many species of phytoplankton produce DMS which assists in the formation of clouds. It has been thought that the Earth’s climate is partly regulated by variations in DMS emissions [103]. Coccolithophores are single-celled calcified algae which produce DMS, but are also capable of increasing the absorption of CO2 from the atmosphere when they bloom. Blooms of coccoliths remove large quantities of carbonate from surface waters which results in increased absorption of CO2 from the atmosphere. When the blooms are dense and the cells die, they may sink to the floor of deep sea areas thereby effectively removing carbon dioxide from the biosphere. This latter process can only operate over deep water and under bloom conditions, which do not occur every year. When water conditions are favourable, species may have the capacity to occur in massive blooms, sometimes > 100,000 square kilometres (the size of England) in extent. Some species of phytoplankton produce and liberate toxins and may form Hazardous Algal Blooms (HABs) when they are present at high densities. These are potentially damaging to human and animal health and therefore have some economic importance. There is extremely high diversity of planktonic organisms in the waters of the UK, while we can identify some species that discharge key roles, e.g. toxic species, Calanus as food of herring, the carbon sequestration of coccolithophores the majority of ecological functions provided by the plankton are the result of the diversity of types of organisms present. Benthos Relatively few benthic (animals which live on or in the sea floor) species are harvested within the UK waters, but species of high economic importance include Norway lobsters (Nephrops norvegicus), brown shrimps (Crangon crangon), cockles (Cerastoderma edule), mussels (Mytilus edulis) and scallops (Pecten maximus). Benthic invertebrates can form a substantial proportion of the diet of commercially important fish. Crustaceans, polychaete worms and echinoderms are major components of the diet of Atlantic cod (Gadus morhua) [104], haddock (Melanogrammus aeglefinus) [105], dab (Limanda

limanda) [106], plaice (Pleuronectes platessa), sole (Solea solea), [107]and the long rough dab (Hippoglossodies platessoides) [108]. Important benthic organisms include habitat formers and bioturbators (animals which mix and turbate the sediment). Habitat formers increase the complexity of their environment and so promote habitat diversity (one of the levels of biological diversity) [109]. Habitat forming benthic invertebrates are known to increase the species richness and the abundance of individuals present in an area. Examples of habitat forming species which increase diversity include bivalves such as mussels [110, 111], cold water reef building corals (e.g. Lophelia) [87, 112-114] and reef or tube building polychaete worms (Sabellariidae and Lanice conchilega) [115, 116]. Bioturbating species are functionally important as they assist the recycling of nutrients between the sea floor and the water column. Bioturbators turn over the sediment, pump oxygenated water into it and enhance the microbial decomposition of the organic matter which falls out of the water column. The result of these processes is that decomposition and hence the supply of nutrients in coastal seas is strongly related to these benthic bioturbators. Examples of bioturbators are the large crustacean species (belonging to Callianassidae) and large burrow forming polychaete worms. Fish Although cod (Gadus morhua), haddock (Melanogrammus aeglefinus), whiting (Merlangius merlangus) and saithe (Pollachius virens) are targeted heavily by the fishing industry, and are therefore of economic importance, they are also of significant ecological importance and can form up to 80% of the total biomass of the demersal fish eating predators. Other ecologically important fish species include herrings and sandeels, which are important both as prey and predator, and some non-target fish, such as dab, which consume a significant proportion of the benthic animals and so make the production available to higher predators. Several fish species are considered to be important by society and include cod, several elasmobranch species (sharks, rays and skates) and seahorses. These have been included on the OSPAR list of threatened and/or declining species. Marine Mammals and Reptiles All cetaceans (whales, dolphins and porpoises) are protected and listed under Annexes II and IV of the Habitats and Species Directive (1992) [41] and are valued by society. Cetaceans provide income from whale/dolphin watching trips and similar eco-tourism initiatives. Within the UK, direct expenditure on this activity was valued at USD$1,844,000 in 1998 with a total expenditure of USD$8,231,000 [117]. Toothed whales (dolphins, porpoises and killer whales) are important predators of marine mammals and fish are of high ecological importance at the top of the food chain. The dominant seal species within the UK are the common seal (Phoca vitulina) and the grey seal (Halichoerus grypus). Both of these species are listed under Annex II of the EU Habitats and Species Directive [41] and are of societal importance. Seals are also important predators of fish and may be of

economic importance as they may compete with fisheries for food resources [118]. Although the evidence for this is patchy and much of it is outdated[118], studies have shown that a substantial proportion of the grey seal’s diet consists of commercially exploited fish species [119, 120]. Marine turtles are protected by the Habitats and Species Directive [41] and UK Biodiversity Action Plan (UK BAP). Leatherback turtles are the most frequently recorded species of turtle in UK waters (94% of records), although the loggerhead, Kemp’s Ridley and hawksbill turtles are also sighted regularly, if infrequently [121]. Although turtles have been sighted in waters all around the UK, they are most frequently encountered in areas to the south-west and west in regions most influenced by the North Atlantic drift. Their low numbers and sporadic occurrence mean that ecologically, they are probably not important ecosystem components in UK waters. Seabirds

The majority of seabird species found in the North Sea are protected under the EC Birds Directive 1979 [122] and the EC Habitat and Species Directive 1992 [41]. Some bird species can be considered of economic importance as they contribute to eco-tourism and recreational biodiversity value. Visitors pay £11.7 million a year to visit RSPB reserves alone [123]. Most seabird species are important as predators occurring at or near the top of the marine food web and so have high ecological importance.

Habitats of importance The habitats listed below are considered important largely for functional or societal reasons. Identifying important habitats was based on their inclusion in international legislation and agreements. The identification of other important habitat types was more difficult due to a lack of basic information. In the absence of any other indicators, functional importance was assigned to habitat types according to their size. These were estimated from maps of marine landscapes (Figure 1). [This assumption is unlikely to be supported for any given function e.g. muddy habitats are more important for nutrient regeneration functions than reefs, but it is a reasonable to assume that the larger and more common habitats will support a high proportion of the functioning than the smaller ones, and will therefore be of greater functional importance]. We have considered only actual habitat types (e.g. mud, sand or rock) here and not the habitats of species (e.g. cod habitat, porpoise habitat or sandeel habitat) as there are few robust data available. The habitat types identified below are from the JNCC Marine Habitat Classification for Britain and Ireland Version 04.05 [124].

Muddy and sandy communities

Cohesive mud and sand habitats form a significant proportion of UK marine habitats. They occur in areas of low hydrodynamic (wave and current) energy (see Figure 1). The infaunal communities (organisms which live within the seafloor sediments) they support are dominated by active (polychaete) worm

and echinoderm (e.g. starfish and brittlestars) assemblages which perform important nutrient recycling functions through their bioturbatory activities [125], are considered important prey for fish, and enhance biodiversity through making the habitat more heterogeneous or patchy [126-128]. Their nutrient recycling ability is especially important in muddy sea beds of low permeability as their activities enhance the transport of liquids back up to the water column at rates significantly greater than simple chemical diffusion alone [129, 130]. This processes enhances the flow of nutrients back up into the water column where they are accessible to phytoplankton.

Sublittoral3 mixed sediment Sublittoral mixed sediments form a significant proportion of UK marine habitats . These habitats support a relatively diverse and abundant benthic fauna which are functionally important as they are involved with nutrient recycling through bioturbation [6, 7, 24], supporting diverse communities by increasing habitat complexity through the creation of tubes and burrows [24, 115, 126, 127, 131] and they are considered an important food resource for commercially important fish [91, 104-106, 132-134]. Sublittoral coarse sediment (unstable cobbles and pebbles, gravels and coarse sands) Sublittoral coarse sediment habitats form a significant proportion of UK marine habitats. The benthic communities which inhabit these sediments tend to be of a lower diversity and abundance [130, 135-138] than the more stable muddy habitats. However, many commercially important fish species utilise, and show preferences for, coarse sedimentary habitats throughout their life history [139-148].

Up to 50% of the organic matter produced in the water column may be decomposed in the seafloor [149]. In marine sands, water can flow through the particles providing a faster exchange of substances between the water column and the upper sediment layers [130]. Permeable sands are efficient filters of particulate organic matter (POM) and act as biocatalysts, accelerating mineralization of organic carbon and recycling nutrients. High flushing rates, preventing build-up of nutrients and refractory particulate organic carbon (POC) in the pore space. North Sea sands are therefore very active sites of nutrient recycling [150].

Sublittoral sands and muddy sands

Sublittoral sands and muddy sands form the largest proportion of UK marine habitats. These habitats are characterised by high densities of polychaete worms, echinoderms, and crustaceans such as small shrimps. These benthic invertebrates are a substantial proportion of the diet of commercially important fish [104-106, 133]. The presence of fine sediment also attracts some species of juvenile flatfish as it allows them to bury into the sediment to avoid predators [151].

3 Permanently underwater

This habitat type supports infauna with strong sediment-disrupting traits. High densities of one tube-building polychaete have been shown to increase the species richness and abundance of other polychaetes in the areas by providing a spatial refuge from predators and improving sediment stability [152]. Sublittoral biogenic4 reefs on sediment Sublittoral biogenic reefs include cold water coral, ross worm and horse mussel reefs which are all listed under the Habitats Directive [41] and the UK BAP, and are identified as threatened and declining by OSPAR [153]. The presence of physically complex habitat types has been demonstrated to support higher abundances [113] and more diverse communities than in adjacent, less structurally complex habitats [87]. Sublittoral algae-dominated communities on sediment Sublittoral algae-dominated habitat types includes maerl beds, sublittoral seagrasses and sublittoral kelp beds. All these habitat types are protected by the UK BAP, and maerl and seagrasses have been identified as threatened and declining by OSPAR, and therefore may be considered of considered of societal importance. These habitat types are known to support assemblages of juvenile fish and shellfish [154-156]. Infralittoral5 rock Infralittoral rock includes areas of bedrock, boulders and cobbles which occur in shallow waters and typically support seaweed (kelp) communities. These seaweeds support high diversities of invertebrates which attracts fish, birds and marine mammals to these areas. Inshore sublittoral rocks have been identified as a broad habitat type by the UK Biodiversity Action Plan which has recommended maintaining ‘the extent and quality of inshore sublittoral rock habitats in the UK, including the full diversity of communities’ [80].

4 Of biological origin 5 Areas which are permanently underwater but within the region of light.

Appendix 2

Trends in the important species and groups of species

Phytoplankton and Zooplankton

Total zooplankton The continuous plankton recorder (CPR) survey provides probably the best combination of spatial and temporal coverage of a marine ecosystem component anywhere in the world. The data are however limited as it is derived from one depth and subject to the influence of the variety of factors that always affect the catch in nets. Bearing these constraints in mind the CPR does provide an excellent comparative tool for looking at changing spatial and temporal patterns in plankton. Since 1946 there have been considerable changes in many ecosystems around the UK with a particular large change, often referred to as a regime shift, around 1982–1988 [157]. In addition to the regime shift there has been a northerly biogeographic movement of warm water plankton of 10° of latitude in forty years and a parallel retreat of cold water plankton to the north [158]. After the mid-1980s the planktonic ecosystem moved from a cold temperate to a warmer dynamic regime around the UK. Total phytoplankton The total level of phytoplankton biomass in UK coastal waters fall below the criteria developed by OSPAR (the Comprehensive Procedure criterion) which triggers detailed analysis of suspected eutrophicated sites. This suggests that in coastal waters the amount of microscopic plants has not responded dramatically to the increased level of nutrients in the sea (from fertilizer runoff and sewage effluent disposal). Data from the CPR however, do suggest marked changes in the species of phytoplankton and the timing and size of the annual growth cycles. This is probably a response to both altered climate patterns (particularly spring warming), altered nutrient balances and altered species of grazing zooplankton. The changes are likely to have resulted in changed patterns of nutrient cycling and food production and so directly impacted on key ecosystem goods and services. Harmful Algal Blooms - HABs Some plankton species are occurring earlier in the season (including dinoflagellates), which has important implications for the monitoring and study of Harmful Algal Blooms (HABs). One of the most studied HABs in the North Sea is the foam alga Phaeocystis. Massive developments of this alga occur regularly in the southern North Sea. The long-term monthly variability of Phaeocystis, averaged for the North Sea, is shown in Figure 2. Whereas it was particularly common in the 1950s, it began a process of decline which lasted through the 1960s and 1970s. Since the mid- 1980s, the occurrence of Phaeocystis has increased in the North Sea, with 1999 standing out as an exceptional year due to a number of large blooms. It has been suggested that increases in Phaeocystis could be attributed to an increase in nitrogen and phosphorus inputs [159]. However, similar patterns of occurrence are found in

other regions of the North-East Atlantic where nutrient levels have not been increased by man, suggesting that the patterns are affected by the climate, mirroring what is seen for phytoplankton biomass. Remarkably similar decadal patterns of abundance have also been observed for the dinoflagellate (a type of marine alga) Noctiluca scintillans from the Helgoland Roads, in the southern North Sea, which have been related to winter sea surface temperature (SST)[160]. Some of the most exceptional phytoplankton blooms recorded by the CPR survey have also been associated with atypical ocean climate conditions and oceanic incursions into the North Sea [54]. Bloom events recorded by the CPR survey also show strong similarities with other phytoplankton surveys [161, 162].

Figure 2. Long term monthly variability of Phaeocystis from CPR records averaged from the North Sea (Source: Defra, 2005 [1]) Emiliana huxleyi Emiliana huxleyi is the dominant coccolithophore (a type of marine alga) in UK waters. Coccoliths are calcified, single celled algae that may provide important climate regulation functions. Blooms of Emiliana huxleyi may be sensitive to climate change [163], and changes have been observed in their global distribution. Coccolithophores appear to be advancing into some sub-Arctic seas, for example the Bering Sea [164], while perhaps becoming more scarce towards the equator. This may be a result of global warming. Calanus finmarchicus Copepods dominate the zooplankton (animal plankton). Calanus is a large copepod which is rich in fats and is important in the diet of many larval fish and a major food item of plankton feeding fish such as herring [165, 166].

Calanus finmarchicus is a northern species and spends the winter in ‘hibernation’ in deep water in the Norwegian Sea and re-enters UK shelf waters in the spring each year. Since around 1960, numbers of Calanus finmarchicus in UK shelf waters have declined. It has been suggested that part of the reason for the decline is attributable to a decrease in the volume of the cold deep water in the Norwegian Sea [167] reducing inflows of water through the Faroe Channel that bring new individuals in spring. The warming of the seas is also likely to have reduced their suitability for this northern species. Higher temperatures, and possible increased flows in the slope current may also have been unfavourable to the recolonisation of shelf seas like the North Sea.

Sea-bed organisms (benthos)

General trends Large scales changes in the benthic communities of the North Sea and Irish Sea have been observed over the last century. These changes have largely been related to human activities such as fishing [168], aggregate extraction [70] and pollution [169, 170]. Several long term studies have observed increases in the occurrence of mobile, robust and scavenging taxa, whilst slow-moving or sessile, fragile taxa have decreased [74-76, 171-173]. These changes were attributed to physical disturbance from the fishing industry and the provision of large amounts of food from discards and moribund benthos on the sea floor. In one of the few studies to directly measure ecological functioning, Bremner et al., (2003) examined how the functions of the benthic communities changed with varied fishing pressure. Biological traits analysis (BTA) links characteristics of the benthos to the functions they provide and was used to examine benthic communities inside and outside a fishing area off NE England. Analysis showed that the functional structure of the two communities were different and that the structure of the community inside the fishing ground changed between 1972-1994 simultaneous with changes in fishing pressure. No changes were observed in the community outside of the fishing ground during this time. Evidence from the Wadden Sea suggests that there have been decreases in organisms with no, or limited, mobility (sponges and bivalves) and an increase in worms between 1869 – 1979 [173]. This change was attributed to the more opportunistic and robust nature of the worms and their higher tolerance to disturbances such as oxygen depletion, severe cold and oil spills. Ocean quahog clam (Arctica islandica) The ocean quahog is a slow growing species and populations of 40-80 year old individuals have been observed [153]. Its growth reflects local food availability [174]. Quahog populations in the North Sea have decreased during the last 100 years [175]. due to their vulnerability to various disturbances to the seabed. Beam trawling is known to cause shell damage [176, 177], and the mortality of quahogs caught in a beam trawl has been estimated to be in

the range of 74-90% [153]. Other threats to quahogs include sand and gravel extraction, and the direct and indirect effects of oil and gas extraction which may result in a decrease in growth rate [174].

Cold water coral (Lophelia pertusa) It is only relatively recently that efforts to investigate the distribution of the cold water coral Lophelia pertusa have been undertaken. For instance, the Darwin Mounds were only discovered in May 1998. However, these corals are sensitive to physical disturbances and trawling is likely to cause mechanical damage, killing the coral polyps and breaking up the reef structure [178]. This makes the habitat much less suitable for the highly diverse communities supported by the reef structure [113, 114]. Trawling may also flatten the seabed by scraping off high points and infilling lows, as well as redistributing boulders. Since this coral seems to require some of the high points to grow initially, the seabed habitat following trawling may become unsuitable for coral growth. Although the Darwin Mounds were not protected immediately after their discovery, and evidence of new damage was observed during the summer of 2000 [179, 180], specific European legislation was introduced to protect the reefs in 2004 [181]. However, photographic and acoustic surveys have located trawl marks over unprotected Lophelia reefs at 200–1400 m depth all along the edge of the Northeast Atlantic shelf slope area of Ireland, Scotland, and Norway [178]. Fish Fishing is a selective process. Fishers aim to capture certain species within a selected size range. This selection is partly the result of market demand, and partly in order to fulfil management restrictions such as minimum landing sizes. Long term data sets have shown that this selective pressure has affected the size structure of the entire North Sea fish community with a reduction in the proportion of fish in the larger classes decreasing between the 1974-1996 [182] and an increase in the abundance of smaller fish over large parts of the North Sea during the last 30 years [183]. Fishing has also changed the species composition of the demersal fish community (fish which tend to occur just above the seabed), such as cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) and flatfish such as plaice (Pleuronectes platessa). Demersal fish communities in three areas around the British Isles were compared between 1901-1907 and 1989-1997 [184]. In Start Bay (NW English Channel) and the Irish Sea, species diversity was the same during both periods, although the most abundant species in each period were not the same. In English coastal regions of the southern North Sea, fish populations became more diverse, as plaice and whiting (Merlangius merlangus) became less abundant, and the relative abundance of several non-target species such as dragonet (Callionymus lyra), bib (Trisopterus luscus), and bull-rout (Myoxocephalus scorpius) increased. Overall, the proportions of larger fish (maximum body length >30 cm) in catches decreased in all regions during the time period, except in the Irish Sea where plaice replaced grey gurnard (Eutrigla gurnardus) as a dominant

species. The proportion of smaller fish present (maximum body length <30 cm), which were considered the least vulnerable to capture, was observed to increase between the two survey periods in Start Bay and the southern North Sea. One study showed that changes in the species composition of demersal fish communities in the North Sea between 1925 and 1996 led to an increase in the mean growth rate, whilst the mean maximum size, age at maturity and size at maturity decreased [185]. Changes in the abundance and composition of the rays, skates and sharks have been observed in the central and north-western North Sea between 1929–1956 and 1981–1995 [186]. Survey data show that some species have decreased in abundance (common skate (Raja batis), and thornback ray (Raja clavata), whilst others (starry ray (Raita radiate)) have increased. The sequence of the five most common species from most to least sensitive is: common skate> thornback ray> spotted ray (Raja montagui) > cuckoo ray (Raja naevus) > starry ray. This is also the order of commercial importance. Similar observations were recorded between 1901-1907 and 1989-1997 [184] with decline in large sharks, skates and rays in areas around the British Isles. These declining species included the common skate, white skate (Raja alba) and the angel shark (Squatina squatina). During 1901-1907 surveys, 60% of the rays and sharks consisted of thornback ray, whereas in the contemporary surveys, the lesser spotted dogfish was the most abundant. Changes in length-frequency distribution of fish in both target and non-target categories, and other observed changes, are consistent with a response to commercial exploitation.

Marine Mammals and Reptiles

Seals The UK holds 39% of the world’s population of grey seal and 90% of these breed in Scotland [187]. The grey seal (Halichoerus grypus) population has grown steadily since the 1960s to an estimated maximum population of 123,000 in 2002. Grey seal pup production increased steadily from 1984– 1996, and has remained broadly static since 2000 (Figure 3). The UK holds approximately 40% of the world population of the European sub-species of common seal. The total population estimate is approximately 50–60,000. Total estimated pup populations have shown an upward trend since 1984 and are probably attributable to management measures including restrictions on hunting and protection of breeding sites [188]

Figure 3. Total estimated grey seal pup production for all major breeding colonies in Scotland and England (excluding Loch Eriboll, Helmsdale and Shetland) from 1984 to 2002. Estimates are within ± 14% of the point estimates. (Source: SOCS, 2003 [187])

Cetaceans Ten species of cetacean (whales and dolphins) occur regularly in UK waters and a further 18 occur infrequently. Population estimates only exist for a few species at more than a local scale (Table 7). In the Moray Firth, the data suggest a stable bottlenose dolphin population [189]. For no other species or population of cetacean are there any reliable information on trends in population size. The SCANS (Small Cetacean Abundance in the North Sea) survey of 1994 provided baseline data on the size of North Sea populations of harbour porpoise, whitebeaked dolphin and minke whales [190]. This survey is currently being repeated (SCANS II – http://biology.st- andrews.ac.uk/scans2/index.html) and will allow trends and changes to distribution to be established.

Table 7: The status of cetacean species occurring regularly in UK waters Species Common Population estimate for UK/ Date of ®ularly adjacent waters? estimate recorded over/near UKCS? Minke whale 9 c. 8,500 (95% CI: 5,000-13,500)in the 1994 Balaenoptera North Sea, Celtic Sea andSkagerrak acutorostrata (Hammond et al., 1995) Sperm whale 9 Physeter macrocephalus Common 9 c. 130 in the Moray Firth (Wilson et al., various bottlenose 1997); c. 130-350 in Cardigan Bay (Lewis dolphin 1992, Arnold et al.,1997); c. 85 in the Tursiops Channel,including north-west France truncates (Liret et al., 1998) Short-beaked 9 c. 75,500 (95% CI: 23,000- 1994 common dolphin 249,000) in Celtic Sea (Hammond et al., Delphinus delphis 1995) and c. 62,000 (95% Cl: 35,500- 108,000) in adjacent Atlantic 1993 waters (Goujon et al. 1993 White-beaked 9 7,856 (95% CI: 4,032-13,301) 1994 dolphin in the North Sea and Channel Lagenorhynchus (Hammond et al., 1995) albirostris Atlantic White- 9 No data available N/A sided dolphin Lagenorhynchus acutus Combined 9 c. 11,760 (95% CI: 5,867-18,528) 1994 Lagenorhynchus in the North Sea, Celtic Sea and species Baltic Sea (Hammond et al., 1995) Risso’s dolphin 9 At least 142 in the northwestern 1999 Grampus griseus Minch (Atkinson et al., 1999)

Killer whale 9 Orcinus orca Long-finned pilot 9 whale Globicephala melas Harbour porpoise 9 c. 280,000 in the North Sea(Hammond et 1994 Phocoena al., 1994) phocoena Source: Defra, 2005 [1]

Turtles Most turtle species are threatened and in decline throughout their global distribution [121]. Godley et al (1998) [191] discuss the cause of mortality of 35 leatherback and three loggerhead turtles recorded around the British coast from 1992-96. In at least six cases, leatherbacks were known to have drowned after having become entangled in fishing gear. Cause of death was not known for most stranded animals, but evidence suggestive of previous entanglement was present in several cases. Stranded animals were distributed widely around the coasts of northern and western Britain. A conspicuous clustering of strandings and bycatch was identified in Carmarthen Bay, SW Wales. This was thought to have been associated with the rapid expansion of a pot fishery for whelks [121]. Seabirds Changes in seabird populations have included substantial (>10%) declines in the occurrence of two species (herring gull and roseate terns) as well as clear evidence of recovery in other species (e.g. great skua, common guillemot, arctic skua, northern gannet, lesser black-backed gull, northern fulmar, common gull, razorbill, atlantic puffin, great cormorant, little tern, sandwich tern) following the introduction of protective measures [1]. Two examples are provided below:

Black-legged Kittiwakes Since the late 1960s, the number of breeding black legged kittiwakes (Rissa tridactyla) in colonies in the UK has declined by around 7%. This decline has been most rapid in the last decade and the late 1990s-early 2000s with a series of very poor breeding seasons. Analysis of the breeding success with sandeel fisheries data showed a strong negative correlation (Figure 4)[192]. This prompted the introduction of fisheries management measures to limit this effect with the fishery regulated on the basis of the black-legged kittiwake breeding success. Subsequent studies have shown that while the fishery was limiting the number of older, larger, sandeels, the birds were feeding on small fish that were not taken by the fishery. Poor breeding has also continued in recent years even though the fishery has been closed since 1999 (Figure 5). This suggested that competition with the fishery was not the main factor causing the decline in black-legged kittiwake breeding at most colonies with some data suggesting that sandeels are now smaller and less oily than in the recent past, and thus of less nutritional value and is probably related to poor feeding conditions for the sand eels caused by climatically driven changes in zooplankton productivity [193]. This example illustrated how changes in the global climate patterns can be translated through the ecosystem to impact on the top predator, in this case kittiwakes.

120 1.4

100 1.2 ) t r i 0 1 a 0 80 0 P

1 r

( 0.8 e 60 ngs

0.6 ks p c i

ndi 40 0.4 h C La 20 0.2

0 0

6 8 0 8 0 2 8 8 9 92 94 96 9 0 0 9 9 9 9 0 0 1 1 1 19 19 19 1 2 2 Year

Sandeel Landings Chicks per Pair

Figure 4: Trends in the kittiwake breeding success EcoQ metric determined for between 2 and 7 colonies along the east coast of Scotland between Troop Head and St Abbs and sandeel catch from the closure area. (Source: Tasker and Furness, 1996 [194])

Skuas Populations of great skuas (Stercorarius skua) have increased by about 200% since the late 1960s. In common with most seabirds, this is the result of reduced persecution/hunting, lower levels of contaminants and the discarding of fish and fish offal by the fishing industry. Great skuas feed by stealing food from other birds. In particular around the breeding colonies they attack feeding kittiwakes and auks causing them to release the sandeels they have just captured. Offshore a large part of their diet comprises fishery discards, both offal and undersized and non-target fish. Tasker and Furness (1996) [195] estimated that in the North Sea seabirds consume annually 100,000 tonnes of discards and 70,000 tonnes of offal, mainly from the demersal whitefish fishery (i.e. cod, haddock and whiting). Future fisheries management practices will seek to lower discards, particularly of small fish. This is likely to affect smaller species of scavenging seabirds most, e.g. great skuas, herring gulls and lesser black-backed gulls [196]. There is evidence that great skuas are increasingly feeding on other seabirds and the proportion of seabirds in their diet is higher in years when fewer discards are produced by the North Sea whitefish fishery and when sandeel stocks are low [197]. The numbers of seabirds taken by great skuas can be considerable at some colonies [198], and they are having a significant impact on some populations of Arctic skuas, black-legged kittiwakes and Leach’s storm-petrel [199].

0 Group Sandeels

900 s

e 800 n

n 700 o 600 Fishery 500 1000 t Seabirds

s ( 400 Fish Preds

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R 100 0 1963 1966 1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 Year

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e 3500 n n

o 3000 2500 Fishery

1000 t 2000 Seabirds s ( 1500 Fish Preds val

o 1000 m e 500 R 0 1963 1966 1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 Year

Figure 5: Long-term trends in the utilisation of the 0 group and 1+ group sandeel resource by industrial fisheries and fish and seabird predators based on data derived from the MSVPA (Source: ICES, 2004 [145])

Trends in the important habitats Little information is available to provide robust information on the status and trends of larger habitat types found in UK marine waters. Although there is a significant body of work on the effects of fishing on various habitat types [22, 131, 200-228], the majority of these studies have been conducted over very small spatial and temporal scales and at global different locations and are therefore of limited use for determining the overall status and trends of the habitats.

Cohesive mud and sandy mud Little information exists on status and trends of this habitat type in offshore areas. The level of natural disturbance it encounters is relatively low, so recovery from any human impacts is likely to be on the scale of months to years. Experimental trawling of a muddy area closed to fishing for 25 years showed that there were still differences in the biological communities after 18 months, despite the smoothing of the surface sediment [229].

Sublittoral mixed sediment Little information exists on the status and trends of this habitat type in offshore areas.

Sublittoral coarse sediment (unstable cobbles and pebbles, gravels and coarse sands) Sublittoral coarse sediment is extracted as aggregate and data are available to assess the impact of this activity. Aggregate extraction occurs mainly off the east and south east coasts of England at a relatively stable rate of around 23 million tonnes per annum [1]. This rate is likely to increase in future years following the discovery of substantial aggregate resources in the Eastern English Channel, which could provide resources for at least 25 years at current levels of demand and provide >50% of the predicted future requirements [1]. Studies have shown that the benthic fauna exposed to high dredging intensities remained in a perturbed state for 4 years after the cessation of dredging [70]. Distinct differences still persisted in assemblages at sites exposed to high and lower levels of dredging intensity for at least 6 years after ceasing of dredging. Clear gradients of change were also observed with increasing distance from the dredging activity [88]. However another study showed full recovery two years after the extraction of aggregate [71]. The reasons for these differences in recovery are unknown but may relate to site specific differences in exploitation history.. Sublittoral sands and muddy sands Little information exists on status and trends of this habitat type in offshore areas. Experimental trawling in Canada, found trawling on sandy sediments reduced surface sediment structures caused by organisms (e.g. tubes or worm casts) and the abundance of flocculated matter [227]. Recovery of the sediment surface took one year.

Sublittoral biogenic reefs on sediment Most biogenic reefs have a relatively slow rate of recovery from disturbance, and some may be destroyed by a single impact event [230]. Cold water coral reefs The main known areas of cold water coral reef (Lophelia sp.) in UK waters are the Darwin Mounds and areas around the Rockall Bank (see 9.1.2). The Darwin Mounds were designated a Special Area of Conservation (SAC) and are specifically protected by European legislation following the identification of

fishing as a threat to this habitat[181]. The cold water coral reefs around Rockall are, as yet, unprotected, although signs of fishing damage are visible and there are concerns about hydrocarbon extraction in the area [87, 178]. The impacts of the latter activity are uncertain. Horse mussel beds Horse mussel (Modiolus modiolus) beds are identified by the UK BAP as a priority habitat, and recognised as threatened and declining by OSPAR (2005)[153]. Trawling has been observed to remove emergent epifauna, such as dead man’s fingers anemones (Alcyonium digitatum), and disrupt horse mussel clumps to give an overall flattened appearance to the beds in Strangford Lough [231]. This activity also reduces the habitat complexity of the horse mussel bed and affects the communities. Trawling reduces the habitat complexity of horse mussel beds which in turn, affects the species associated with them (including clams, sea urchins, anemones, starfish, shrimps, whelks and scallops. Worm reefs Some marine worms build tubes from sand and mud or by excreting calcium carbonate. In some species dense aggregations of tubes can form reefs. There is evidence that serpulid worm reefs in Loch Creran has been adversely affected by the discharge from the organic rich effluent from a factory and from the physical disturbances caused by boat moorings [232]. However, scallop dredging was considered the most significant threat to Serpulid worm reefs in this area.Elsewhere, shrimp trawling has been shown to cause no visible damage to ross worm (Sabellaria spinulosa) reefs [84]. Sublittoral algae-dominated communities on sediment Although there is evidence of long-term damage to maerl beds in France, there is little information on historic trends in the extent of UK maerl beds. Threats to maerl have been identified however. Barbera et al., (2003) [83] identified the direct and indirect threats to maerl as: 1) Physical impacts e.g. reduction in light penetration due to sediment resuspension, such as when sediment is dumped or sewage discharged; alteration of inshore currents such as caused by coastal structures; burial of live maerl by land reclamation or towed demersal fishing gears; changes in the nature of the sediment with an increase in the finer silt-clay particles. 2) Chemical impacts e.g. increase in organic matter and in nutrients (the latter leading to eutrophication), as caused by sewage outfalls, below and in the vicinity of aquaculture units, and when sediment is re- suspended by towed demersal fishing gears. 3) Biological impacts e.g. decrease in habitat complexity, as when the physical structure associated with maerl-associated algae is altered, resulting in a decrease in species richness and abundance; changes in species composition, such as to more opportunistic species; the substitution of hard-bottom species with soft bottom ones, or the substitution of indigenous biota by alien species.

In Scotland, there have been extensive studies on the effects of fishing on maerl beds which have shown reductions in the complexity, biodiversity and long-term viability of maerl beds [82, 154, 233]. Experimental dredging showed that five months after scallop dredging, there were 70-80% fewer live algal foliage than in control areas and there were no signs of recovery over the following four years[82]. The sculpted ridges and troughs of the dredge tracks remained visible for between 1.5-2.5 years. These were gradually erased through bioturbation by large infauna. In France, the uncontrolled spread of slipper limpets (Crepidula fornicata) is also a problem to maerl [234]. Dense aggregations of this snail trap suspended silt and faeces and the maerl structures become clogged with silt which kills them.

Infralittoral rock Infralittoral rock includes areas of bedrock, boulders and cobbles which occur in the shallow subtidal zone and typically support seaweed communities. The upper and lower limits of this habitat type tend to be marked by the zone of seaweed. In exposed conditions the kelp is Laminaria hyperborea whilst in more sheltered habitats it is usually Laminaria saccharina. Laminaria hyperborea habitats support diverse and abundant invertebrate communities. The invertebrate fauna supported by NE Atlantic kelps are dominated by crustaceans and molluscs [235-238]. Invertebrate abundance is particularly high in the kelp holdfasts (the ‘roots’ of the kelp) and associated with epiphytes (encrusting organisms) on the stipes (the ‘stalk’ of the kelps) [239]. A study by Christie et al. (2003) showed that 56 individual plants of Laminaria hyperborea supported 238 species, with an average density of almost 8000 individuals per kelp. This diverse fauna may be important as food for predators such as otters, fish, crabs, lobsters and seabirds both in the kelp and in adjacent communities [239-242]. The kelp also provides a physically complex habitat for juvenile fish [243, 244]. Approximately 87% of the 3,000 hectares of rocky shore SSSIs in the UK were considered to be in a favourable condition [245].