WORKING GROUP on SEABIRD ECOLOGY. ICES CM 2001/C:05, Ref

Oceanography Committee ICES CM 2001/C:05 Ref.: E,F and ACME

REPORT OF THE

WORKING GROUP ON SEABIRD ECOLOGY

ICES Headquarters 16–19 March 2001

This report is not to be quoted without prior consultation with the General Secretary. The document is a report of an expert group under the auspices of the International Council for the Exploration of the Sea and does not necessarily represent the views of the Council.

International Council for the Exploration of the Sea Conseil International pour l’Exploration de la Mer

Palægade 2–4 DK–1261 Copenhagen K Denmark

TABLE OF CONTENTS Section Page

1 INTRODUCTION...... 1 1.1 Participation ...... 1 1.2 Terms of Reference ...... 1 1.3 Justification of Terms of Reference...... 1 1.4 Overview by the Chair...... 2 1.5 Note on bird names...... 2 1.6 Acknowledgements ...... 3 2 STATUS OF MARINE BIRDS IN THE NORTH SEA...... 3 2.1 Seabirds in the North Sea ...... 3 2.2 Summary of trends in status of seabirds in the North Sea ...... 3 2.3 Wildfowl Wintering in or Migrating Through the North Sea...... 7 2.4 Summary of Trends for Wintering and Migratory Divers, Grebes and Wildfowl in the North Sea...... 7 2.5 Waders Wintering in the North Sea...... 9 2.6 Summary of Trends of Numbers of Waders Wintering in the North Sea...... 9 2.7 References and Sources Used in Tables...... 11 3 ECOLOGICAL QUALITY OBJECTIVES FOR SEABIRDS IN THE NORTH SEA...... 12 3.1 Introduction ...... 12 3.2 Contaminants...... 14 3.3 Fisheries ...... 29 3.4 Habitats and ecosystem health...... 31 3.5 Hunting/harvesting ...... 33 3.6 Disturbance...... 33 3.7 Introduced/conflicting species...... 33 3.8 Climate change...... 34 4 FURTHER DEVELOPMENT OF SEABIRD MONITORING ...... 34 4.1 Introduction ...... 34 4.2 Demands for the parameters and seabird species selected for monitoring ...... 35 4.3 Seabirds as sensitive indicators for change in the marine environment: Monitoring characteristics of seabird life history besides population size...... 36 4.4 Seabird diets and provisioning as monitors of fish stocks and food availability...... 41 4.5 Recommendations for further monitoring marine pollution using seabirds as accumulative indicators ...... 41 4.6 Further aspects of designing monitoring programmes with seabirds ...... 42 4.7 References ...... 43 5 REVIEW OF THE INTERACTIONS BETWEEN AQUACULTURE AND BIRDS IN THE ICES AREA...... 47 5.1 Introduction ...... 47 5.2 Enhancing food supplies to wildlife ...... 47 5.3 Attraction of birds to aquaculture and consequent impacts on fish farming profitability...... 49 5.4 Disturbance of birds by aquacultural activities ...... 50 5.5 Persecution of birds by fish farmers...... 50 5.6 Impacts on birds of the harvest of mussel spat...... 52 5.7 Impacts of industrial fishing on seabirds...... 52 5.8 References ...... 58 6 FURTHER REVIEW OF THE CONTENTS ON THE DATABASE ON SEABIRD DIET COMPOSITION...... 61 7 WHAT QUESTIONS CAN WE TRY TO ANSWER DURING CONCURRENT MEETINGS WITH OTHER WORKING GROUPS? ...... 61 8 RECOMMENDATIONS...... 62 8.1 Proposal for next meeting...... 62 8.2 Proposal for a Cooperative Research Report...... 63 8.3 Chair...... 64 8.4 Request to other groups for information...... 65 8.5 Proposal for a Mini-Symposium ...... 65 ANNEX 1 – NAMES AND ADDRESSES OF PARTICIPANTS ...... 66 ANNEX 2 – SCIENTIFIC NAMES OF SPECIES USED IN THIS REPORT ...... 67 @#

1 INTRODUCTION

1.1 Participation

The nominated members of the Working Group who participated in the meeting are listed in Annex 1.

1.2 Terms of Reference

At the 87th Statutory Meeting, it was agreed that the Working Group on Seabird Ecology [WGSE] should meet in ICES Headquarters from 16–19 March 2001 (4 days) (C.Res. 1999/2CSE). The terms of reference were to: a) respond to the following requests from OSPAR [OSPAR]: i) provide a synthesis of the status of North Sea populations of seabirds, including consideration of species that have declined or are threatened by human activities; ii) consider the use of seabirds as indicators for environmental quality and short-term and long-term ecosystem effects; iii) provide recommendations for appropriate EcoQO indices for seabirds based on i) and ii) and make suggestions for appropriate EcoQOs for North Sea seabird populations (with WGECO and SGEAM); iv) prepare provisional estimates for the current levels, reference levels and target levels for the EcoQO indices identified (with WGECO and SGEAM). b) examine the practicality and desirability of monitoring other aspects of seabird life history than those presently monitored; c) review interactions between mariculture and birds in the ICES area; d) continue to compile a first model of food consumption by seabirds for the entire ICES area; e) assess the inter-sessional work of continuing to add to the database of seabird diet or forage prey composition in the ICES area; f) further develop ideas for meetings that might be held concurrently with other Working Groups in 2003;

The Working Group on Seabird Ecology will report by 16 April 2001 for the attention of Oceanography, Marine Habitat and Mariculture Committees and ACME.

1.3 Justification of Terms of Reference a) These four Terms of Reference have been formulated from the OSPAR Work Programme for 2001. In providing the recommendations requested under (iii), account should be taken on the outcome of the Oslo workshop on ecosystem approach including the background document prepared for the workshop, the outcome of the Scheveningen workshop on EcoQOs as well as a number of other documents including the report from a short planning meeting for all EcoQOs held by ICES in October 2000. b) A start on this process was made in 2000 when the sensitivity of seabird population to changes in life history parameters was made. At present, parameters monitored include breeding numbers and success. The process in 2000 indicated that adult survival was particularly important for long-lived species dynamics, while age at first breeding was important for shorter-lived seabirds. This work will complement that carried out under a). c) The Working Group has not examined this area previously, and such a review will help support the development of mariculture in an ecologically sustainable manner as well as enhance the usefulness of the Working Group in further parts of the ICES structure. d) The Working Group has been modelling consumption for a number of years, with a view to developing a model of the whole ICES area in due course. The information should be of interest to other ICES Working Groups, as well as to OSPAR and HELCOM. e) The Working Group is keen to add information on energy density of prey species and different length/age classes to its database and will be searching for this information (see 2) below). f) The Working Group is keen to continue the process of integration of seabird ecology into the workings of ICES. We look forward to possible concurrent working with sister Groups under the Oceanography Committee umbrella. It is considered that a similar process would be productive for groups working under other committees.

1.4 Overview by the Chair

The Working Group met for four days (16–19 March 2001), and was attended by ten nominated representatives from seven countries (Annex 1). It was able to address all but one term of reference and the results are reported here.

The first term of reference was a response to a request to ICES from OSPAR and concerned the development of Ecological Quality Objectives (EcoQOs) for seabirds in the North Sea. In this context it was assumed that “seabirds” meant all birds reliant on the quality of the North Sea for a significant part of their life cycle; thus an attempt was made to include shorebirds and nearshore waterbirds, such as duck, along with the more traditional offshore seabirds. However members present had only limited experience of these inshore bird species. The question of EcoQOs was approached from the angle of the manager of activities in the marine environment of the North Sea. Thus an attempt was made to answer the question that a manager might pose “What can seabirds best tell me about the quality of the marine ecosystem and its status, and what should I be aiming to achieve when measured using a seabird-based parameter?” The Working Group has carried out several reviews of the usefulness of seabirds as monitors of the marine environment. Seabirds provide good evidence of the changing levels of contamination and pollution in the North Sea, particularly in relation to oil, mercury and various xenobiotic substances. Seabirds may also provide a suitable way of monitoring plastic particle pollution. In relation to fisheries, it is known that seabirds are sensitive to changes in food supply, and are being used as a proxy measure of the size of prey fish stock within the North Sea. On the basis of this knowledge, it is suggested that EcoQO indices be developed for these features and some provisional estimates of levels for these indices have been made. A broad EcoQO for the seabird community was also suggested, using this EcoQO as a trigger for further analysis should any population of seabird decline in size by a certain proportion. This EcoQO would apply also for threatened and declining species.

The Working Group considered that, at the present level of knowledge, seabirds would not provide ideal EcoQOs for eutrophication, by-catch in fisheries, discards from fisheries, mariculture, disturbance or climate change in the North Sea.

Suggestions for the further development of seabird monitoring were reviewed. In an ideal world the most important extra parameters to monitor beyond those commonly undertaken are immature and adult survival rates: these factors have a great influence on population size. However, monitoring of these parameters is at present relatively difficult and resource intensive. The monitoring of contaminant loads in seabirds will aid in studies of pollution in the environment.

The Working Group carried out a review of the interaction of mariculture and birds in the ICES area. The aim of this review is to provide to ICES, and specifically to the ICES Working Group on Environmental Interactions of Mariculture, a brief review from the perspective of seabird ecologists, of the interactions between aquaculture and birds. There has been a huge growth in aquaculture in the last few decades, with consequent concerns for a variety of environmental impacts. Aquaculture can enhance food supplies to wildlife, sometimes at the expense of fish farming profitability; can disturb or persecute birds; impact birds through the harvest of mussel spat or through industrial fishing. The Working Group is aware also that wild birds can be vectors of diseases that affect cultured fish and shellfish but did not have the expertise to review this issue.

We did not address the term of reference on further assessing food consumption of seabirds within the ICES area at this meeting. This was partly due to pressure of time and partly due to the absence of key members of the group who have been working on this area over a number of years. However, intersessional work by group members has led to the preparation of a manuscript to be submitted to an externally refereed journal on food consumption in Norwegian waters.

There have been few further developments of the database on seabird diet composition that has been assembled by the Working Group. We had few further suggestions in relation to working concurrently with other Working Groups, but draw attention to our request in the 2000 Report (CM 2000/C:04) for information on the energy density of fish and other seabird prey.

1.5 Note on bird names

Keen-eyed readers of the past reports of this Working Group will note a change in English names of many of the birds mentioned. Most of these changes have come through the addition of an adjective to an already existing name (e.g., lapwing to northern lapwing). These changes are in line with those agreed a few years ago by the British Ornithologists’ Union and are now in line with the nomenclature used by most European English-language ornithological journals. A full list of species names with their scientific binomial appears in Annex 2.

1.6 Acknowledgements

The Working Group wishes to thank ICES and their staff for providing rooms for our meeting, computing and photocopying facilities. We thank Henrik Skov, Stefan Garthe, Kees Camphuysen, Theunis Piersma, Daniel Oro, Bill Montevecchi and Rob Barrett (absent members of the group) for their help in supplying information and advice.

2 STATUS OF MARINE BIRDS IN THE NORTH SEA

Marine birds (here including wildfowl and shorebirds as well as traditional seabirds) are some of the more prominent members of the marine community of the North Sea (ICES Divisions IIIa, IVa, b and c, VIId and e), and consequently their numbers are relatively easy to survey. These surveys are reported in a number of places, often on a national basis. A consequence of this is that it is not always possible to provide comparative up-to-date totals of some species. In this chapter, we present information on the current population sizes of seabirds, wildfowl and waders found in the North Sea, and attempt to cast these current numbers in terms of the birds’ historical abundance (which for some species is dramatically different from that at the present). The best information is available for seabird species that breed or for shorebirds and wildfowl that winter around the North Sea. Where possible and appropriate, estimates of other populations are also presented. It is important to know the status of marine birds that occur in the North Sea if they are to be used in setting Ecological Quality Objectives.

2.1 Seabirds in the North Sea

All countries surrounding the North Sea have programmes that collect information on numbers of breeding seabirds. Unfortunately it was not possible to bring together all information on the most recent national estimates of numbers, particularly for the UK (where a complete re-census of colonies is underway). Due to this incompatibility and incompleteness of information between countries, we have used the most recent published estimates of breeding numbers for the whole North Sea (Dunnet et al. 1990). Population estimates of seabirds at sea in the North Sea as a whole have most recently been summarised by Skov et al. (1995). These data were derived from seabird surveys carried out from 1979 to 1994 in the North Sea. Several sampling methods were used to produce estimates of each species at sea over a year: counts from land, aerial total counts, aerial transect counts, ship total counts and ship transect counts. A Geographical Information System mapping routine was used to perform a detailed stratification of species distributions within predefined sectors in the North Sea. Density and population estimation were carried out for each sector while information on numbers of birds that would be expected to be associated with breeding colonies of seabirds in the study region were derived from the United Kingdom Seabird Colony Register and other sources (see Lloyd et al. 1991, Grimmet and Jones 1989, Hälterlein and Steinhardt 1993). These data are presented in Table 2.1 along with an indication of the overall trend of the breeding population in the North Sea. Summaries of trends and geographical variation appear in the text below.

2.2 Summary of trends in status of seabirds in the North Sea

2.2.1 Northern fulmar

Fulmars have increased in numbers in the North Sea quite dramatically since the early part of the 20th century (Fisher 1952). The rate of increase has slowed in the 1990s compared with the 1950s and 1960s. In France (where it first colonised in 1960) the (small) population has stabilised or even decreased slightly in the 1990s, while in the UK the overall increasing trend has also peaked recently in, for example, Shetland. However, significant population growth has occurred in Norway in recent years. The North Sea population increase that had continued rapidly from 1900 to at least 1980 may now have ceased.

2.2.2 Manx shearwater

A breeding bird mainly in western parts of the British Isles, the small population of Manx shearwaters (< 200 pairs) in the Channel increased in the late 1990s. The small population in Shetland has been severely reduced by mammals introduced to its breeding islands.

2.2.3 European storm-petrel

European storm-petrel populations that breed in the Northern Isles of Scotland (probably numbering in the low thousands) have not been adequately surveyed in the past. Their status here is being assessed currently and overall trend data are not available.

2.2.4 Leach's storm-petrel

The status of the very small Leach's storm-petrel population in the North Sea is also poorly known and is also currently being investigated.

2.2.5 Northern gannet

Numbering in excess of 80 000 breeding pairs, northern gannets have been increasing everywhere in the North Sea in recent decades (at a rate of 0.5–3% per annum between 1990 and 1999; Upton et al 2000), probably partly as a result of feeding on discarded fisheries waste. At Runde, Norway, just north of the North Sea, gannets have been increasing steadily by as much as 10% per year since they established there in 1946.

Table 2.1. Population figures for seabirds on North Sea coasts. Wintering counts are of individuals; breeding data are nesting pairs except for auks which are individuals. Breeding data are from Dunnet et al (1990) for all species except northern gannet, the sources here being Murray and Wanless (1997) and Thompson et al. (1996); winter data are from Skov et al. (1995) and are modelled estimates based on known average densities in winter months in different areas of the North Sea. Recent (c. last decade) trends of breeding populations (where known or suspected) are indicated. German trends are from Hälterlein et al. (2000).

Species Wintering population Breeding population Breeding trend

Northern fulmar 3,744,000 307,599 = Manx shearwater 500 c. 250 = European storm-petrel 0 low 1000s Leach’s storm-petrel 0 low 100s? Northern gannet 157,800 60326 + Great cormorant 14,315 2222 + European shag 29115 19804 + Arctic skua 0 3194 - Great skua 1000 7303 + Mediterranean gull 0 c150 + Little gull 5370 40 + Black-headed gull ? 129,342 = Mew gull 175,530 73,332 Lesser black-backed gull 15315 49,311 + Herring gull 971,700 237,114 = Yellow-legged gull ? 10s + Great black-backed gull 299900 24,436 + Black-legged kittiwake 1,032,690 415,427 - Gull-billed tern ? <100 ?- Sandwich tern 0 30,547 = Roseate tern 0 36 - Common tern 0 61,487 = Arctic tern 0 74,729 = Little tern 0 2335 Common guillemot 1,562,400 680,434 ind + Razorbill 324,000 73,115 ind + Black guillemot 6595 23,741 ind = Little auk 852,690 0 Atlantic puffin 26000 (early winter) 225,957 ind + 74600 (late winter)

2.2.6 Great cormorant

Great cormorant populations can fluctuate markedly from year to year. An increase was recorded in French colonies between 1987 and 1998 and there have been large increases (up to 30% growth pa) over the last three decades mainly in Denmark, Germany and the Netherlands (van Eerden and Gregersen 1995). This has been mirrored in southern parts of the UK but northern Scottish (including Orkney and Shetland) populations have shown marked decline over the same period (Budworth et al in press).

2.2.7 European shag

European shag breeding numbers in the North Sea are relatively variable within wide limits. In the last decade there has been some overall population growth in French and Norwegian colonies, while counts at UK North Sea colonies

indicate stability over a similar time period. Colonies in SW Norway have increased, while those in the much larger colony at Runde (just north of the North Sea) have decreased by a mean of 5% per year since 1975 (Figure 2.1).

300

200 150

100 80 60

40 30

20 SW Norway 15 Runde Mean level 10 UK (mean) 8 6

Population size in % of mean count of mean % in size Population 4 3

1975 1980 1985 1990 1995 2000 Year

Figure 2.1 Standardized abundance of nesting pairs of European shags at two Norwegian and five U.K. colonies (data from Lorentsen (2000) and the UK Seabird Colony Register).

2.2.8 Arctic skua

Most arctic skuas breeding around the North Sea do so in Shetland and Orkney, with small populations in Norway and north Scotland. The limited evidence available suggests that after some decades during which numbers increased, numbers have been declining since 1990; for example, at five monitored plots in the Orkney Islands they have declined by 54% since then (Upton et al. 2000).

2.2.9 Great skua

Great skuas are also confined mostly to Orkney and Shetland. Overall, an increase in breeding numbers here has occurred in the past 10 years but there have been some recent, localised decreases.

2.2.10 Mediterranean gull

The Mediterranean gull breeds in France, UK, Netherlands and Germany in increasing numbers.

2.2.11 Little gull

Small, but increasing, numbers of little gulls breed in the Netherlands.

2.2.12 Black-headed gull

Breeding numbers of black-headed gulls at colonies can be variable from year to year but coastal colonies in Scotland have probably declined over the past decade. Larger colonies in eastern England have increased over the same period but the Wadden Sea population seems to have remained relatively stable (Rasmussen et al. 2000).

2.2.13 Mew gull

Over the past five to ten years there have been moderate, localised increases in monitored mew gull colonies in Scotland but overall UK North Sea populations appear to be relatively stable. Numbers in the Wadden Sea almost doubled in a similar time frame but Norwegian populations have declined by around 5–10%per year over the past decade; in some cases these declines have persisted from the 1970s.

2.2.14 Lesser black-backed gull

The most southerly populations of lesser black-backed gulls in the North Sea appear recently to have been relatively stable, for example in France since 1988. However, the species has increased dramatically in the Wadden Sea since 1990 (a total increase of 150% from 1990–1995), and numbers have continued to increase gradually in eastern England. In south-east Scotland (Isle of May) breeding numbers tripled between 1987 and 1999, this following cessation of a cull of breeding adults on the island (Harris et al. 2000). Some colonies in Norway have decreased in recent years but this has been offset by population growth in others. The overall population trend in the North Sea would appear to be one of slight population growth.

2.2.15 Herring gull

Data from the last ten years suggest a levelling off of earlier trends of both population decline and growth in various parts of the North Sea. Wadden Sea populations have declined slightly, while numbers in France have remained fairly stable over the past decade. In most Norwegian areas the species has increased by 6-7% annually since the late 1980s.

2.2.16 Yellow-legged gull

Small, but increasing, numbers of this species, only recently identified as a separate species from herring gull, breed in France, southern England, the Netherlands and Germany.

2.2.17 Great black-backed gull

Breeding numbers of great black-backed gulls increased markedly in Norway (up to 18% per year in some areas) and the German Wadden Sea in the past decade. The limited evidence available suggests that populations elsewhere are increasing slowly. This is true for the southeastern North Sea, notwithstanding a period of population stability in France from 1987–98. Some major colonies in Orkney declined between 1984 and 1997 (Upton et al. 2000); however, there have been some large increases in breeding numbers in Norway since the late 1980s (and earlier).

2.2.18 Black-legged kittiwake

Black-legged kittiwakes have been declining in the North Sea as a whole for the past 15 years or so. A census of the Shetland population in 1999 indicated a decline of 71% since 1981 (Thompson et al. 1999). In north-east Scotland breeding numbers declined by 53%, between 1992 and 1999 (Upton et al. 2000). Similarly, the Isle of May population (SE Scotland) halved between 1990 and 1999 (Harris et al. 2000). Those at Runde (just north of the North Sea) have increased by 4.3% per year since 1980.

2.2.19 Gull-billed tern

Small numbers of gull-billed tern breed on Wadden Sea shores.

2.2.20 Sandwich tern

The available evidence suggests that the North Sea population of Sandwich terns has remained fairly stable since 1990. Local fluctuations probably represent movement among colonies; for example, the peak in numbers in the Wadden Sea in 1994 was coincident with a decline in UK breeding numbers in the same year (Upton et al. 2000).

2.2.21 Roseate tern

Roseate terns continue to retain a precarious hold in the North Sea; nesting pairs ranged from 74 in 1988 to 47 in 1999 (Upton et al. 2000). Some of the recent decline in North Sea populations may reflect emigration to the relatively successful colonies in Ireland.

2.2.22 Common tern

More than 50% of North Sea common terns breed in Norway, where numbers have decreased by 5-15% per year in most areas for the past 10-25 years. Since the 1980s (and earlier) colonies here have significantly decreased in size. Similarly, in the German Wadden Sea numbers have significantly decreased in the last decade. In the UK, population size appears to have increased, while in France it has remained stable over the same time. The extent to which the variation in breeding numbers reflects movement between colonies is not known.

2.2.23 Arctic tern

The population of arctic terns in the North Sea is probably relatively stable following a large decline in the early 1990s.

2.2.24 Little tern

Around half of North Sea little terns breed in the Wadden Sea. Over the last 10 years the population in the German Wadden Sea has increased significantly; no data on population trends in Denmark trends are available. Numbers in both France and the UK also appear to have grown modestly.

2.2.25 Common guillemot

The great majority of common guillemots in the North Sea breed in the UK. Here they have increased markedly since the mid-1980s; in south-east Scotland and north-east England, annual population growth was 3.9% and 4.8% respectively (Upton et al. 2000). The small population in France has also been increasing since 1955. Common guillemots at Runde (just north of the North Sea) have decreased by 2.2% per year since 1980.

2.2.26 Razorbill

Although few data are available from the smaller colonies in the Channel, at Helgoland and in Norway, UK data indicate that razorbills have increased in the North Sea over the past 15 years. Scottish colonies as a whole have increased at between 3.1 % and 41% per year since 1986 (Upton et al. 2000).

2.2.27 Black guillemot

The few data available suggest that black guillemot numbers in the North Sea have remained relatively stable over the past 15 years.

2.2.28 Atlantic puffin

The small Atlantic puffin population in the Channel has remained stable over the last decade, but breeding numbers on the UK coasts of the North Sea have increased greatly over the last 15 years. Numbers at Runde have increased slightly since 1980.

2.3 Wildfowl Wintering in or Migrating Through the North Sea

The status and trends in numbers of divers, grebes and selected wildfowl wintering in the North Sea were identified by Skov et al. (1995). Populations for several seasons were available for some species, and so the season with the highest population total has been reported in Table 2.2. Data for Brent goose, long-tailed duck and shelduck were extracted from Delaney et al. (1999) using protocols described for wintering waders (see Section 2.5). The status and population trends of wintering wildfowl on North Sea coasts are shown in Table 2.2

2.4 Summary of Trends for Wintering and Migratory Divers, Grebes and Wildfowl in the North Sea

2.4.1 Divers and grebes

The status of divers and grebes in the North Sea is given in Table 2.2. Approximately 50,000 red- and black-throated divers, 14,000 great-crested and 2,000 red-necked grebes winter in the North Sea, predominantly inshore along southern North Sea coasts and Kattegat (Skov et al. 1995). Great-northern divers are rare with only 900 birds wintering in the region, mostly along sheltered rocky coasts in the far north-west of the North Sea. The regular monitoring of wintering

seabirds in Norway has documented a significant decrease in numbers of red-necked grebes in Rogaland (Anker- Nilssen et al. 1996). For other North Sea areas there are no available data on trends in the numbers wintering.

2.4.2 Brent goose

Approximately 227, 000 Brent geese winter in the North Sea, these being from populations that breed in Svalbard and Siberia. They are mainly distributed among the larger estuaries in the southern North Sea. The populations are increasing following a population reduction caused by hunting and a disease affecting Zostera, their main food plant. (Scott and Rose 1996).

2.4.3 Common shelduck

The number of shelducks in the North Sea is approximately 114,000 (derived from data in Delaney et al. 1999, Pollit et al. 2000). Shelducks occur in estuarine habitats and so are mainly found in the southern North Sea. Almost the entire north-west European population gathers in the Wadden Sea to moult (Scott and Rose 1996). The population increased by 50% between the late 1960s and late 1980s, but is now thought to be stabilising (Scott and Rose 1996). Pollit et al. (2000) show that common shelducks along North Sea coasts in the UK were approximately stable over the last decade.

Table 2.2 Peak numbers of divers, grebes and wildfowl on North Sea coasts during winter; figures are individual birds in 1994/95. Data are from Skov et al. (1995) for most species but from Delaney et al. (1999) for Brent goose, long-tailed duck and shelduck.

Species Peak numbers in winter Trend

Red-and Black-throated diver 48495 Great northern diver 905 Great crested grebe 13900 Red-necked grebe 1975 Brent goose 227000 + Common shelduck 114000 = Greater scaup 13665 Common eider 462590 Long-tailed duck 11576 = Black scoter 570310 = Velvet scoter 121430 = Common goldeneye 16400 + Red-breasted merganser 9855 = Goosander 3230 =

2.4.4 Greater scaup

There are approximately 14,000 scaup wintering in the North Sea, with the majority of these occurring in the Kattegat, Firth of Forth and Voordelta (Skov et al. 1995). Trends over the whole North Sea are unknown, although the numbers in the Firth of Forth have declined following reductions in discharge of waste grain from distilleries (Kirby et al. 1993).

2.4.5 Common eider

The population of common eiders wintering in the North Sea numbers approximately 462,600 birds, with most of these occurring in the Kattegat and along shallow coasts along the Wadden Sea and the Scottish firths (Skov et al. 1995). Overall trends of birds wintering in the North Sea are unknown, although declines have recently been recorded in the Dutch Wadden Sea following collapses in the stocks of the species’ shellfish prey.

2.4.6 Long-tailed duck

Long-tailed duck numbers in the North Sea were approximately 11600 birds (Delaney et al. 1999), although this is probably an underestimate owing to many birds being offshore when land-based counts are conducted (Pollit et al. 2000). Kirby et al. (1993) estimated the population as around 20,000 birds. Within the North Sea, they are concentrated in the Scottish firths, particularly the Moray Firth (Pollit et al. 2000). Their populations are unknown but are believed to be stable (Scott and Rose 1996).

2.4.7 Black and velvet scoter

There are approximately 570,000 black scoters and 121,000 velvet scoter wintering in the North Sea. The majority of these spend the winter in the Kattegat, west Danish coast, Wadden Sea and Voordelta (Skov et al. 1995). Their populations are reported to be stable (Scott and Rose 1996).

2.4.8 Common goldeneye

The number of goldeneye wintering in the North Sea is approximately 16400, with most birds being found in the Kattegat, Voordelta and British estuaries and coasts (Skov et al. 1995). A large proportion of the north-west European population winters on freshwater lakes and reservoirs and numbers at sea are increased considerably during freezing weather. The numbers wintering in north-west Europe has increased over the last decade by as much as 50% (Scott and Rose 1996).

2.4.9 Red-breasted merganser

The number of red-breasted mergansers wintering in the North Sea is approximately 10,000 birds (Skov et al. 1995) and these were mainly found in British estuaries and firths. The population wintering in north-west Europe is believed to be relatively stable (Scott and Rose 1996).

2.4.10 Goosander

Approximately 3200 goosander winter in the North Sea (Skov et al. 1995), and a large proportion of the European wintering population inhabit freshwater lakes and reservoirs and the Baltic Sea. The population wintering in north-west Europe is considered to be largely stable (Scott and Rose 1996).

2.5 Waders Wintering in the North Sea

Wintering waders and wildfowl are counted every month between September and March in the UK (organised by the Wildfowl and Wetlands Trust, the British Trust for Ornithology, the Royal Society for the Protection of Birds and the Joint Nature Conservation Committee) and more widely in January as part of the International Waterbird Census (co- ordinated by Wetlands International).

Data from these schemes were extracted for the winter of 1994–95 from Delaney et al. (1999) and Pollit et al. (2000). This year provided the only available snapshot of wader numbers during a typical winter (1996 data are available in Delaney et al. (1999), but this was a relatively cold winter and waders may have moved into the Irish Sea, thereby rendering the results from that year somewhat atypical). Counts represent summed peak counts rather than average counts, and so will represent overestimates, particularly for more mobile wader and waterfowl species. Delaney et al. (2000) provide country totals, and since some countries have estuarine coasts outside the North Sea (UK and France), the totals over-estimate species status in the North Sea. Wader count data from the Atlantic coast of France could not be excluded from the North Sea total. However, estuary counts were available for the UK (Pollit et al. 2000), allowing west British counts to be excluded from the North Sea totals. Hence, the wader totals for the British North Sea coast were calculated by summing the totals counted at estuaries on the east coast and Channel in the winter of 1994–95. These represent numbers only at internationally or nationally important sites and do not include numbers of waders dispersed among smaller, less important sites (e.g., sanderling). Further analyses of the original data would be required to improve these estimates. It should be noted also that the numbers of waders using North Sea coasts on migration and in winter comprise only a small component of the meta-populations of these species, which use wider European/African/ Asian migratory flyways. The status and trends of wintering wader populations on North Sea coasts is shown in Table 2.3.

2.6 Summary of Trends of Numbers of Waders Wintering in the North Sea

2.6.1 Eurasian oystercatcher

Numbers of Eurasian oystercatchers have gradually increased since the 1970s in the UK and the population was larger than in all previous years in 1997. The Wadden Sea holds almost half of the north-west European total, and the UK holds about 30%. In 1995 and 1996, numbers in the Wadden Sea declined somewhat and this decline was matched by increases in France, the non-Wadden Netherlands and the UK. This shift in abundance is almost certainly the result of recent cold winters.

2.6.2 Ringed plover

Populations of ringed plovers have generally been stable since the 1970s. However, numbers in the UK have been dropping since the early 1990s following peak abundance in 1990. A particularly sharp decline in the UK was recorded between 1998 and 1999.

2.6.3 European golden plover

In 1995–1996, the distribution of European golden plovers shifted from the UK towards France and the Netherlands. This shift presumably reflected the harsh winter of 1995–1996. No long-term change in the North Sea population is evident.

Table 2.3. Status and trends of selected wintering estuarine waders on the North Sea coast in 1994/95. Note that these are peak migratory counts, so may be overestimates. Data are from Delaney et al. (1999) and Pollit et al. (2000).

Species Population Trend

Eurasian oystercatcher 772,000 +/= Ringed plover = European golden plover = Grey plover 77,000 + Northern lapwing = Red knot 219,000 = Sanderling 11,000 = Dunlin 656,000 = Black-tailed godwit + Bar-tailed godwit 62,000 = Eurasian curlew 289,000 +/= Common redshank 30,000 = Common greenshank + Ruddy turnstone =

2.6.4 Grey plover

There has been a long-term increasing trend of grey plovers in the UK, amounting to over 50% since 1970. In the cold winters of 1995–1996, fairly substantial shifts away from the Wadden Sea towards France and the non-Wadden Netherlands was noted. These were local shifts in abundance that do not appear to have impacted the long-term increasing trend however.

2.6.5 Northern lapwing

The North Sea populations of northern lapwings appear to be stable, despite a shift in range east and south following cold winters.

2.6.6 Red knot

Populations of red knots in the UK and in the Wadden Sea are either stable or declining slightly. A decline is more evident in the Wadden Sea, and the decline there may reflect extensive shellfish harvesting by humans, which disturbs the birds’ feeding grounds.

2.6.7 Sanderling

In the UK the sanderling populations have fluctuated considerably since 1969, but there does not appear to be any long- term trend. Substantial increases in France and the Wadden Sea in 1995–1996 more than compensated for decreases in the UK.

2.6.8 Dunlin

Populations of dunlins in the North Sea area have not displayed any trend since 1969, though there have been local fluctuations that seem to reflect eastward and southward movement to avoid cold winters.

2.6.9 Black-tailed godwit

Black-tailed godwits have been increasing in western Europe for most of the 20th century. This increasing trend is still apparent in the UK and Wadden Sea.

2.6.10 Bar-tailed godwit

Bar-tailed godwits have fluctuated in abundance, but no trend is apparent for the North Sea area since 1969. As with many waders, birds move from the Wadden Sea to the UK and to the south during cold winters.

2.6.11 Eurasian curlew

There has been an increasing trend in Eurasian curlew populations between about 1980 and 1995. In 1995, numbers decreased in the UK and Wadden Sea, as well as in other parts of western Europe. It is not clear whether these declines represent shifts to the south, due to missing data. Numbers seem to have increased again in the UK in 1998, but then declined in 1999. Nevertheless the 1999 number in the UK is equal to the 1969–1999 mean.

2.6.12 Common redshank

Common redshank populations have been stable since 1969. There have, however, been decreases in 1995–1996 in the whole North Sea area. These declines seem to be related to the cold winter, and the numbers have not completely recovered in these areas. Nevertheless, 1998–1999 yielded totals close to the 1969–1999 mean.

2.6.13 Common greenshank

Common greenshanks have been increasing as a passage migrant in the UK over the last ten years.

2.6.14 Ruddy turnstone

Ruddy turnstone numbers in the UK have been declining since about 1989, when a peak was recorded. Counts in the U.K. in 1999 were close to the 1969–1999 mean. Recent decreases in UK numbers seem to have been compensated for by increases in France and the non-Wadden Netherlands.

2.7 References and Sources Used in Tables

Anker-Nilssen, T., Erikstad, K. E. and Lorentsen, S.-H. 1996. Aims and efforts in seabird monitoring: an assessment based on Norwegian data. Wildlife Biology 2: 17-26.

Budworth, D., Canham, M, Clark, H., Hughes, B. and Sellers, R. M. 2001. Status, productivity, movements and mortality of great cormorants Phalacrocorax carbo breeding in Caithness, Scotland: a study of a declining population. Atlantic Seabirds In press.

Delaney, S., Reyes, C., Hubert, E., Phil, S., Rees, E., Haanstra, L. and van Strien, A. 1999. Results from the International Waterbird Census in the Western Palaearctic and Southwest Asia 1995 and 1996. Wetlands International Report.

Dunnet, G. M., Furness, R. W., Tasker, M. L. and Becker. P. H. 1990. Seabird ecology in the North Sea. Netherlands Journal of Sea Research 26: 387–425.

Fisher, J. 1952. The fulmar. Collins, London

Grimmet, R. F. A. and Jones, T. A. 1989. Important bird areas in Europe. International Council for Bird Preservation, Cambridge. Technical Publication 9.

Hälterlein, B. and Steinhardt, B. 1993. Brutvogelbestände an der deutschen Nordseeküste im Jahre 1991 – Fünfte durch die Arbeitsgemeinschaft ‘Seevogelschutz’. Seevögel 14: 47–51.

Hälterlein, B., Südbeck, P., Knief, W., Köppen, U. 2000. Brutbestandsentwicklung der Küstenvögel an Nord- und Ostsee unter besonderer Berücksichtigung der 1999er Jahre. Vogelwelt 121: 241–268.

Harris, M. P., Wanless, S., Darling, I. and Gallacher, C. 2000. Breeding birds of the Isle of May, Firth of Forth, 1972– 99. Scottish Birds 21: 6–14.

Heath, M., Borggreve, C. and Peet, N. (compilers) 2000. European bird populations: estimates and trends. BirdLife International, Cambridge (BirdLife Conservation Series No.10). 160pp.

Kirby, J. S., Evans, R. and Fox, A. D. 1993. A review of the status and distribution of wintering seaducks in Britain and Ireland. Aquatic Conservation 3: 105–137.

Lloyd, C., Tasker, M. L. and Partridge, K. 1991. The status of seabirds in Britain and Ireland. Poyser, London.

Lorentsen, S-H. 2000. Det nasjonale overvåkningsprogrammet for sjøfugl. Resultater til og med hekkesesongen 2000. – NINA Oppdragsmelding 670: 1–30.

Murray, S. and Wanless, S. 1997. The status of the gannet in Scotland in 1994–95. Scottish Birds 19: 10–27.

Pollit, M., Cranswick, P., Musgrove, A., Hall, C., Hearn, R., Robinson, J. and Holloway, S. 2000. The wetland bird survey 1998–99 wildfowl and wader counts. British Trust for Ornithology/The Wildfowl and wetlands Trust/Royal Socirty for the Protection of Birds and Joint Nature Conservation Committee, Slimbridge.

Rasmussen, L. M., Fleet, D. M., Hälterlein, B., Koks, B. J., Potel, P., and Südbeck, P. 2000. Breeding birds in the Wadden Sea in 1996. Common Wadden Sea Secretariat, Wilhelmshaven, 123 pp.

Scott, D. A. and Rose, P. M. 1996. Atlas of Anatidae populations in Africa and western Eurasia. Wetlands International Publication No. 41. Wetlands International, Wageningen.

Skov, H., Durinck, J., Leopold, M.F. and Tasker, M.L. 1995. Important bird areas for seabirds in the North Sea. BirdLife International, Cambridge.

Südbeck, P. and Hälterlein, B. 1999. Brutvogelbestände an der deutschen Nordsee küste im Jahre 1997 - Elfte Erfassung durch die Arbeitsgemeinschaft "Seevogel schutz". Seevögel 20: 9–16.

Thompson, K. R., Pickerell, G. and Heubeck, M. 1996. Seabird numbers and breeding success in Britain and Ireland, 1995. Joint Nature Conservation Committee, Peterborough. UK Nature Conservation, No. 20.

Thompson, K. R., Pickerell, G. and Heubeck, M. 1999. Seabird numbers and breeding success in Britain and Ireland, 1998. Joint Nature Conservation Committee, Peterborough. UK Nature Conservation, No. 23.

Upton, A. J., Pickerell, G. and Heubeck, M. 2000. Seabird numbers and breeding success in Britain and Ireland, 1999. Joint Nature Conservation Committee, Peterborough. UK Nature Conservation, No. 24. van Eerden, M. R. and Gregersen, J. 1995. Long-term changes in north-west European population of cormorants Phalacrocorax carbo sinensis. Ardea 83: 61–79.

3 ECOLOGICAL QUALITY OBJECTIVES FOR SEABIRDS IN THE NORTH SEA

3.1 Introduction

The concept of ecological quality objectives (EcoQOs) has been discussed in a number of documents and at a number of recent meetings (Anonymous 1999, Lanters et al. 1999, Kabuta and Enserinck 2000, ICES 2001). Several key features of an EcoQO may be derived from these discussions. These can be summarised as follows:

EcoQOs

• should improve or maintain ecological quality

• should be sensitive to a manageable human activity • should have a relatively tight linkage in time to that activity • should be relatively easily measured • should have a high response to the signal from human activity compared with the variation induced by other factors • should be measurable in a reasonably large proportion of the area to which the EcoQO is to apply • should preferably have been measured over a number of years to provide a baseline of information and allow a realistic setting of objectives • may relate only to the species for which the objective is being set (intrinsic) • may be an indicator of a wider ecological condition (indicator)

The Working Group considered that there were two main directions from which EcoQOs might be derived. One direction would be to examine each seabird species or group of species in turn to see if a relatively easily measured metric relating to that species might be usable as an indicator of ecological condition. The other direction was to examine broad categories of ecological effects of human activities in the North Sea and discuss whether seabirds could provide a suitable EcoQO as an indicator of that effect.

The group decided to follow the second line of approach, and reviewed the OSPAR JAMP (Joint Assessment and Monitoring Programme) categories (with sub-categories by WGSE): a) Contaminants i) oil ii) other contaminants b) Eutrophication c) Litter i) plastic particles d) Fisheries i) by-catch of seabirds ii) harvesting of seabird food iii) provision of seabird food e) Mariculture f) (Marine) habitats and Ecosystem Health

The group felt that these categories did not cover the following human activities (or their effects) that can also affect seabirds in the North Sea. g) Harvesting/hunting h) Disturbance i) Introductions/conflicting species j) Climate change

The usefulness of seabirds as indicators of environmental quality and short- and long-term environmental effects of human activities were discussed in relation to each of these categories and where the group considered it appropriate, recommendations for EcoQO indices were made. Provisional estimates for the current level, the reference level (in this case, the level likely prior to the relevant human impact) and the target level are also provided. EcoQOs other than those presented here were considered for some of the categories in some detail and could be developed further. For instance, we considered whether common terns and Eurasian oystercatchers might provide suitable EcoQOs for their prey species. However, only those the group considered to be the most robust are presented in this report.

The group had considerable difficulty in setting reference and target levels. Reference levels refer to a state without the effects of human activity – this state is easy to know for a few parameters (e.g., pollutants not occurring in nature), but much more difficult in relation to a biological resource (such as a stock of fish) that will be affected not only by a directed activity (e.g., removal) but also to an unknown extent indirectly by links through the food chain.

In relation to target levels, there are no hard scientific facts or rules – these levels are a matter of societal choice and public acceptability. We have attempted to suggest levels that we believe are achievable by current management in the short or medium term and that appear to represent progress towards a goal that we believe society and the public to want. We acknowledge that we are not experts in management of human activities in the maritime environment and it may be that we have overestimated the capability of management systems.

3.1.1.1 References

Anonymous 1999. Workshop on Ecological Quality Objectives (EcoQOs) for the North Sea. Workshop Proceedings 1– 3 September 1999, Scheveningen, Netherlands, Temanord Fisheries Environment. Copenhagen.

ICES 2001. Report of the planning group for the ecological quality objective requests. ICES CM 2001/ACME:01, Ref: ACFM, ACE

Kabuta, S. and Enserinck, L. 2000. Development of indicators for the Dutch North Sea – project GONZ. ICES CM 2000/ACME:WP7

Lanters, R. L. P., Skjoldal, H. R., Noji, T. T., Daan, N., Offringa, H. R., van Gool, S. and van Dam, C. J. F. M. 1999. Ecological Quality Objectives for the North Sea. Basic document for the workshop on Ecological Quality Objectives for the North Sea, 1–3 September 1999. RIKZ Report 99.015. National Institute for Coastal and Marine Management, The Hague.

3.2 Contaminants

3.2.1 Oil pollution

EcoQO title: An index of oil pollution of the North Sea

3.2.1.1 Background

The use of dead or dying seabirds found on beaches as indicators of oil pollution at sea has been reviewed in a number of recent publications (Camphuysen and van Franeker 1992, Dahlmann et al. 1994, Camphuysen 1995, 1998, Wiens et al. 1996, Furness and Camphuysen 1997, ICES 1999). There is evidence to show that the proportion of oiled beached seabirds gives a reasonable index of the numbers of oil slicks at sea, although factors such as wind direction and numbers of seabirds dying from starvation or disease can confound the picture in the short-term (Stowe 1982). However, surveys of beached seabirds provide clear evidence of long-term trends in oiling rates of seabirds (Figure 3.1) and variation in oil impacts between regions (Figure 3.2).

Standards for conducting beached bird surveys have been established by OSPAR (OSPAR 1995), but nevertheless surveys around the North Sea could be more frequent and better co-ordinated, perhaps on a monthly basis. Currently only one international survey occurs each year (in February), with surveys at other times being more systematic in some countries than others. Monitoring is already included in the Trilateral Monitoring and Assessment Programme (TMAP) in the Wadden Sea.

Figure 3.1. Trends in oil rates in razorbills, common guillemots, black-legged kittiwakes and Larus gulls stranded at the mainland coast in The Netherlands, 1979–1995. Data from Camphuysen (1995).

Figure 3.2. Variation in proportion of beached common guillemots that are oiled (oil rate) in western Europe. Data from Camphuysen (1995).

3.2.1.2 Robustness of proposed EcoQO

The proportion of beached common guillemots that are oiled broadly reflects the density of shipping traffic in the North Sea (Figure 3.2) and can be used as an index of oil pollution in the waters used by common guillemots. There have been clear reductions in this proportion and that of other species in one area adjacent to some of the main shipping lanes in the North Sea (Figure 3.1). This reduction reflects efforts in the Netherlands and more widely to reduce oil pollution from shipping. There appears to be a reasonably tight linkage in time between the efforts to reduce oil pollution and the decreasing proportion of oiled birds, although data on the proportion of oiled beached birds are only available after efforts to reduce oil discharges started.

This proposed EcoQO index would be relatively easy to measure and has a reasonably long history. As can be seen in Figure 3.1, the index is subject to short-term variation. Thus a number of years of data would be required before further trends could be detected, or before managers could be sure that they were moving towards or achieving the EcoQO target level. Camphuysen and van der Meer (1995) indicate that a decrease in oil pollution will be detected with a probability of 90% after about 14 years, although for some species this time may be nine years. There are two main known sources of noise in the data, major oil pollution incidents and major non-oiling mortality events (“wrecks”). The former will inflate proportions oiled, while the latter will deflate any index. Camphuysen et al (1999) reviewed mass mortality incidents (including large-scale oiling incidents) and showed that in the ICES area these occurred mostly in autumn and winter and that common guillemot was the most frequently affected species. An EcoQO index of the proportion of beached common guillemots that are oiled could be applied across the North Sea.

3.2.1.3 Discussion

Total seabird mortality from small, frequently unattributable, oil slicks is believed to be higher than that from the larger high profile oil spills that attract great public attention. Nevertheless, no studies have been able to document there are, at present, any measurable effects of oil pollution on the overall populations of seabirds in the North Sea. This proposed EcoQO index is therefore designed to monitor longer-term trends in background oil pollution rather than its effects on seabird populations.

It was noted that some oil spills can have a large effect on more localised populations of seabirds. An example of this occurred in the Firth of Forth where a spill of around 1200 litres of oil led to the deaths of more than 1000 seabirds, many of which were comparatively rare in the North Sea. The numbers of some species of birds killed compared with those known previously to be in the area were high and it is likely that there was an impact on total numbers in the Firth of Forth for a number of years afterwards (no monitoring actually occurred). However, it would be difficult to set EcoQOs based on absolute numbers killed in any incident due to a number of factors. First, there is insufficient information on the biological sub-division of seabird populations in the North Sea. Secondly, in most instances it is impossible to know accurately the total number of birds that have been killed in any one incident as the proportion of birds killed that arrive ashore may be heavily influenced by weather conditions (Stowe 1982).

A further use of beached birds in aiding in the managed reduction in oil spills comes through the chemical fingerprinting of oil from carcasses. This permits the identification of the source of oil on birds and can also be used in prosecutions for discharge of oil at sea (Dahlmann et al. 1994), and can be used to provide guidance to where efforts to further reduce oil pollution might be best targeted.

All species of seabird are collected during beached bird surveys, but common guillemot represents the best species to provide an index of oiling as they represent a large proportion of the overall number of birds, they are widely distributed and are relatively susceptible to oiling as they spend most of the time on the water rather than flying. The EcoQOs have therefore been developed based on oiling rates of common guillemot. It might prove possible to use further, more ecologically restricted species, to monitor oil pollution in narrower niches of the North Sea ecosystem.

3.2.1.4 Provisional Estimates for an EcoQO in the North Sea

Proportion of oiled common guillemots among those found dead or dying on beaches

Reference level: 0%

Although there are a very few natural oil seeps in the North Sea, the level of oiling likely to be attributed to these will not be detectable from beached guillemots. Therefore the reference level prior to human influence is 0%.

Current levels: 12–85%: There is wide geographical variation in oiling rates of guillemots in the North Sea (Figure 3.2).

Target level: 10%: to be achieved in all areas of the North Sea.

The overall objective is a reduction in levels of oil pollution in the environment. It is probably impossible to reduce oil spills to zero. WGSE therefore believes that a 10% oiling rate is an achievable and practical target level in the medium term. The wide geographical variation of current levels of oiling in the North Sea will make this target more easily achieved in some areas than others. Oil pollution that affects seabirds comes from a variety of sources including all forms of shipping, from oil exploration, production and transport, and from land-based sources. All of these sources of oil will need to be addressed to meet this EcoQO target level.

3.2.1.5 References

Camphuysen, C. J. 1995. Beached birds in the Netherlands as indicators of marine oil pollution. Sula 9 (special issue), 1–90. [In Dutch with English summary]

Camphuysen, C. J. 1998. Beached bird surveys indicate decline in chronic oil pollution in the North Sea. Marine Pollution Bulletin 36, 519–526.

Camphuysen, C. J. and van der Meer, J 1995. Recent trends in oiled birds. Appendix 2 to JAMP guidelines on standard methodology for the use of beached birds as indicators of marine oil pollution. OSPAR Commission Monitoring Guidelines 1995–6

Camphuysen, C. J. and van Franeker, J. A. 1992. The value of beached bird surveys in monitoring oil pollution. Technische Rapport Vogelbescherming 10. Nederlandse Vereniging tot Bescherming van Vogels, Zeist. 191pp.

Camphuysen, C. J., Wright, P. J., Leopold, M., Hüppop, O. and Reid, J. B. 1999. A review of the causes, and consequences at the population level, of mass mortalities of seabirds. Pp 51–63 in Furness, R. W. and Tasker, M. L. Diets of seabirds and consequences of changes in food supply. ICES Cooperative Research Report No. 232.

Dahlmann, G., Timm,. D., Averbeck, C., Camphuysen, C. J. and Skov, H. 1994. Oiled seabirds - comparative investigations on oiled seabirds and oiled beaches in the Netherlands, Denmark and Germany (1990–1993). Marine Pollution Bulletin 28, 305–310.

Furness, R. W. and Camphuysen, C. J. 1997. Seabirds as monitors of the marine environment. ICES Journal of Marine Science 54, 726–737.

ICES 1999. Report of the Working Group on Seabird Ecology, ICES Headquarters, March 1999. ICES CM 1999/C:5.

OSPAR 1995. JAMP guidelines on standard methodology for the use of beached birds as indicators of marine oil pollution. OSPAR Commission Monitoring Guidelines 1995–6.

Stowe, T. J. 1982. Beach bird surveys and surveillance of cliff-breeding seabirds. Nature Conservancy Council, CSD Report, 366. Nature Conservancy Council, Peterborough. 207 pp.

Wiens, J. A., Crist, T. O., Day, R. H., Murphy, S. M. and Hayward, G. D. 1996. Effects of the Exxon Valdez oil spill on marine bird communities in Prince William Sound, Alaska. Ecological Applications 6, 828–841.

3.2.2 Mercury

EcoQO title: Seabird eggs and feathers as an index of mercury contamination of marine food chains in the North Sea

3.2.2.1 Background

Mercury is a highly toxic metal that is introduced into the environment by human activities at a rate that exceeds natural inputs (Fitzgerald 1995, Fitzgerald and Mason 1998). High levels in foods are a health hazard to humans, especially in

some marine fish (Monteiro et al. 1996). Mercury concentrations tend to increase up food chains, and are much higher in most marine food chains than in most terrestrial or freshwater ones (ICES 1999). Mercury concentrations are high in seabird eggs and in seabird feathers (Lewis et al. 1993, Monteiro and Furness 1995, Becker et al. 1998). Many studies demonstrate that mercury concentrations in seabird eggs and feathers reflect dietary intake (Lewis and Furness 1991, 1993, Burger 1993, Becker et al. 1993a, 1993b, Stewart et al. 1997, Monteiro et al. 1998, Bearhop et al. 2000a, 2000b, 2000c, Monteiro and Furness 2001), though this is complicated by a pattern of storage of mercury in soft tissues between moults and excretion of most of the body burden of mercury into growing feathers during the moult (Furness et al. 1986, Braune and Gaskin 1987a, 1987b, Hario and Uuksulainen 1993), which in most seabirds occurs primarily after the breeding season. Mercury levels in seabird eggs provide a very reliable measure of trends over years in local contamination (Fig 3.3), since seabirds feed close to their breeding colony during the period of egg formation. This also makes eggs very suitable for comparisons between localities (Fig 3.4) as well as over periods of years (Thyen and Becker 2000). Mercury levels in body feathers reflect mercury in the seabird diet over the summer period prior to moult (Thompson and Furness 1989, Furness et al. 1986, Bearhop et al. 2000c). By selecting particular seabird species with clearly defined diets, it is possible to monitor mercury contamination in a range of food chains. For example, some seabirds feed predominantly on epipelagic fish, other species feed on mesopelagic fish, others on intertidal molluscs, and so on (Monteiro et al. 1995, Thompson et al. 1998a, 1998b). Analysis of body feathers of seabird study skins in museum collections has demonstrated changes in mercury contamination over the last 150 years in a number of food chains and geographical regions, including the North Sea (Figure 3.5) (Thompson et al. 1992a, 1992b, 1993a, 1993b, 1998a, Furness et al. 1995, Monteiro and Furness 1997, Monteiro et al. 1999).

Figure 3.3. Temporal trends in mercury contamination of Eurasian oystercatcher and common tern eggs from selected breeding sites of the Wadden Sea (TMAP). FW=fresh weight of egg content. From Thyen and Becker (2000).

Figure 3.4. Spatial variation in mercury contamination of common tern eggs in 1996 and 1997 from breeding sites of the Wadden Sea (TMAP). Mean concentrations and (ng/g fresh weight of egg content) and 95% confidence intervals are presented. N= 10 eggs each. From Becker et al. 1998.

Figure 3.5. Mercury concentrations in body feathers of Atlantic puffin from south-west Britain and Ireland from 1850 to 1990. From Thompson et al. (1992a).

3.2.2.2 Robustness of proposed EcoQO

Mercury levels in birds are measured using a well-established methodology (Appelquist et al. 1984, Thompson and Furness 1989, Burger 1993, Becker et al. 1994, Bearhop et al. 2000a) and the close relationship between levels in birds and in their food is widely documented (Monteiro et al. 1998, Monteiro and Furness 2001). The literature on mercury in seabirds is very extensive and detailed. Unlike fish and marine mammals, seabirds do not show accumulation of mercury with age (once fully grown – levels in chicks are usually lower than in adults though in a few species levels are higher in chicks), so sampling does not need to take account of bird age except to separate chicks and older birds (Furness et al. 1990, Thompson et al. 1991). The use of seabird eggs to monitor mercury is already implemented in the current TMAP monitoring project in the Wadden Sea (Figures 3.3, 3.4). Some relevant JAMP guidelines exist (OSPAR 1997).

3.2.2.3 Discussion

Certain fish stocks have mercury levels above WHO guidelines, and human health hazards from consumption of food high in mercury are a matter of concern. Given that mercury input to ecosystems tends to be predominantly anthropogenic and that analysis of feathers from seabird study skins shows approximately a 4-fold increase in mercury levels over the last 150 years in many North Sea seabirds, an EcoQO to reduce mercury contamination should be a high priority, and the analysis of seabird eggs and body feathers provides a robust way to measure trends in mercury contamination.

3.2.2.4 Provisional estimates for EcoQOs in the North Sea

Mercury concentrations in eggs of selected seabird species Mercury concentrations in body feathers of selected seabird species

Reference level:

Reference levels can be obtained from body feathers of seabirds collected before 1900. These reference levels vary considerably between seabird species, depending on diet and trophic status, and to a small extent between regions according to local natural sources of mercury (e.g., upwelling of Atlantic water). For many UK seabirds reference levels (defined as levels in birds collected before 1900) are about one quarter of the current levels in each species.

Current level:

Current levels of mercury vary between seabird species and between regions. For common terns in the Wadden Sea in 1997 (Figure 3.3) they varied between 275 and 1016 ng/g fresh mass in egg contents. For Eurasian oystercatchers in the Wadden Sea in 1997 (Figure 3.3) they varied between 169 and 353 ng/g fresh mass in egg contents. For seabird body feathers current levels are reported in a large number of recent publications. Examples for body feathers of adult seabirds include great skua mean 7 mg/kg fresh mass feather (over 100 sampled), increasing by 0.4% p.a. 1900–2000; northern gannet 8 mg/kg fresh mass feather, increasing by 0.3% p.a. 1900–2000, black-legged kittiwake 3.3 mg/kg, common guillemot 1 mg/kg. More pelagic species (e.g., Atlantic puffin) show higher rates of increase, around 1–1.5% p.a. In the southern North Sea, herring gulls showed high rates of increase of mercury contamination up to the 1960s, but show subsequent reductions.

Target level:

The target level should be the reference level for mercury in seabird feathers. In the case of eggs, it is difficult to set a target level since reference levels are not known.

3.2.2.5 References

Appelquist, H., Asbirk, S. and Drabæk, I. 1984. Mercury monitoring: mercury stability in bird feathers. Marine Pollution Bulletin 15: 22–24.

Bearhop, S., Phillips, R .A., Thompson, D. R., Waldron, S. and Furness, R. W. 2000a. Variability in mercury concentrations of great skuas Catharacta skua: the influence of colony, diet and trophic status inferred from stable isotope signatures. Marine Ecology Progress Series 195: 261–268.

Bearhop, S., Waldron, S., Thompson, D. R. and Furness, R. 2000b. Bioamplification of mercury in great skua Catharacta skua chicks: the influence of trophic status as determined by stable isotope signatures of blood and feathers. Marine Pollution Bulletin 40: 181–185.

Bearhop, S., Ruxton, G. D. and Furness, R. W. 2000c. Dynamics of mercury in blood and feathers of great skuas. Environmental Toxicology and Chemistry 19: 1638–1643.

Becker, P. H., Furness, R. W., Henning, D. 1993a. Mercury dynamics in young common terns (Sterna hirundo) from a polluted environment. Ecotoxicology 2: 33–40.

Becker, P. H., Furness, R. W. and Henning, D. 1993b. The value of chick feathers to assess spatial and interspecific variation in the mercury contamination of seabirds. Environmental Monitoring and Assessment 28: 255–262.

Becker, P. H., Henning, D. and Furness, R. W. 1994. Differences in mercury contamination and elimination during feather development in gull and tern broods. Archives of Environmental Contamination and Toxicology 27: 162–167.

Becker, P. H., Thyen, S. Mickstein, S., Sommer U. and Schmieder, K. R. 1998. Monitoring pollutants in coastal bird eggs in the Wadden Sea. Final report of the pilot study 1996–1997/Wadden Sea Ecosystem 8. Common Wadden Sea Secretariat Wilhelmshaven: 55–101.

Braune, B. M. and Gaskin, D. E. 1987a. A mercury budget for the Bonaparte’s gull during autumn moult. Ornis Scandinavica 18: 244–250.

Braune, B. M. and Gaskin, D. E. 1987b. Mercury levels in Bonaparte's gull (Larus philadelphia) during autumn moult in the Quoddy Region, New Brunswick, Canada. Archives of Environmental Contamination and Toxicology 16: 539– 549.

Burger, J. 1993. Metals in avian feathers: Bioindicators of environmental pollution. Reviews in Environmental Toxicology 5: 203–311.

Fitzgerald, W. F. 1995. Is mercury increasing in the atmosphere? The need for an atmospheric mercury network. Water, Air and Soil Pollution 80: 245–254.

Fitzgerald, W. F. and Mason, R. P. 1998. The case of atmospheric mercury contamination in remote areas. Environmental Science and Technology 32: 1–7.

Furness, R. W., Muirhead, S. J. and Woodburn, M. 1986. Using bird feathers to measure mercury in the environment: relationships between mercury content and moult. Marine Pollution Bulletin 17: 27-30.

Furness, R. W., Lewis, S. A. and Mills, J. A. 1990. Mercury levels in the plumage of red-billed gulls Larus novaehollandiae scopulinus of known sex and age. Environmental Pollution 63: 33–39.

Furness, R. W., Thompson, D. R. and Becker, P. H. 1995. Spatial and temporal variation in mercury contamination of seabirds in the North Sea. Helgolanders Meeresunters 49: 605–615.

Hario, M. and Uuksulainen, J. 1993. Mercury load according to moulting area in primaries of the nominate race of the lesser black-backed gull Larus f. fuscus. Ornis Fennica 70: 32–39.

ICES 1999. Report of the Working Group on Seabird Ecology. ICES CM1999/C:5.

Lewis, S. A. and Furness, R. W. 1991. Mercury accumulation and excretion in laboratory reared black-headed gull Larus ridibundus chicks. Archives of Environmental Contamination and Toxicology 21: 316–320.

Lewis, S. A. and Furness, R. W. 1993. The role of eggs in mercury excretion by quail Coturnix coturnix and the implications for monitoring mercury pollution by analysis of feathers. Ecotoxicology 2: 55–64.

Lewis, S. A., Becker, P. H. and Furness, R. W. 1993. Mercury levels in eggs, internal tissues and feathers of herring gulls Larus argentatus from the German Wadden Sea. Environmental Pollution 80: 293–299.

Monteiro, L. R. and Furness, R. W. 1995. Seabirds as monitors of mercury in the marine environment. Water, Air and Soil Pollution 80: 851–870.

Monteiro, L. R., Furness, R. W. and del Nevo, A. J. 1995. Mercury levels in seabirds from the Azores, mid-North Atlantic Ocean. Archives of Environmental Contamination and Toxicology 28: 304–309.

Monteiro, L. R., Costa, V., Furness, R. W. and Santos, R. S. 1996. Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environments. Marine Ecology Progress Series 141: 21–25.

Monteiro, L. R. and Furness, R. W. 1997. Accelerated increase in mercury contamination in North Atlantic mesopelagic foodchains as indicated by time-series of seabird feathers. Environmental Toxicology and Chemistry 16: 2489–2493.

Monteiro, L. R., Granadeiro, J. P. and Furness, R. W. 1998. Relationship between mercury levels and diet in Azores seabirds. Marine Ecology Progress Series 166: 259–265.

Monteiro, L. R., Granadeiro, J. P., Furness, R. W. and Oliveira, P. 1999. Contemporary patterns of mercury contamination in the Portuguese Atlantic inferred from mercury concentrations in seabird tissues. Marine Environmental Research 47: 137–156.

Monteiro, L. R. and Furness, R. W. 2001. Kinetics, dose-response, and excretion of methylmercury in free-living adult Cory’s shearwaters. Environmental Science and Technology 35: 739–746.

OSPAR. 1997. JAMP guidelines for monitoring contaminants in biota. 9/6/97, OSPAR Commission, London.

Stewart, F. M., Phillips, R. S., Catry, P. and Furness, R. W. 1997. Influence of species, age and diet on mercury concentrations in Shetland seabirds. Marine Ecology Progress Series 151: 237–244.

Thompson, D. R. and Furness, R. W. 1989. Comparison of the levels of total and organic mercury in seabird feathers. Marine Pollution Bulletin 20: 577–579.

Thompson, D. R., Hamer, K. C. and Furness, R. W. 1991. Mercury accumulation in great skuas, Catharacta skua of known age and sex, and its effects upon breeding and survival. Journal of Applied Ecology 28: 672–684.

Thompson, D. R., Furness, R. W. and Walsh, P. M. 1992a. Historical changes in mercury concentrations in the marine ecosystem of the north and north-east Atlantic Ocean as indicated by seabird feathers. Journal of Applied Ecology 29: 79–84.

Thompson, D. R., Furness, R. W. and Barrett, R. T. 1992b. Mercury concentrations in seabirds from colonies in the northeast Atlantic. Archives of Environmental Contamination and Toxicology 23: 383–389.

Thompson, D. R., Becker, P. H. and Furness, R. W. 1993a. Long-term changes in mercury concentrations in herring gulls Larus argentatus and common terns Sterna hirundo from the German North Sea coast. Journal of Applied Ecology 30: 316–320.

Thompson, D. R., Furness, R. W. and Lewis, S. A. 1993b. Temporal and spatial variation in mercury concentrations in some albatrosses and petrels from the Subantarctic. Polar Biology 13: 239–244.

Thompson, D. R., Furness, R. W. and Monteiro, L. R. 1998a. Seabirds as biomonitors of mercury inputs to epipelagic and mesopelagic marine food chains. Science of the Total Environment 213: 299–305.

Thompson, D. R., Bearhop, S., Speakman, J. R. and Furness, R. W. 1998b. Feathers as a means of monitoring mercury in seabirds: insights from stable isotope analysis. Environmental Pollution 101: 193–200.

Thyen, S. and Becker, P.H. 2000. Aktuelle Ergebnisse des Schadstoffmonitorings mit Küstenvögeln im Wattenmeer. Vogelwelt 121: 281–291.

3.2.3 Organochlorines

EcoQO title: Seabird eggs as an index of organochlorine pollution of the North Sea

3.2.3.1 Background

Marine pollution with environmental chemicals is a worldwide problem, endangering marine organisms and ecosystem health. Persistent toxic substances such as organochlorines, which decompose only slowly, are of special concern. These substances may affect all ecosystem levels and are addressed by this EcoQO. Other aspects of seabird biology may be harmed, for instance reproduction may be impaired through eggshell thinning or through embryonic mortality (e.g., Furness 1993, Becker et al. 1993).

The use of seabirds as monitors of marine contamination with organochlorines such as PCBs, DDT and metabolites, HCB, HCH and others has been advocated many times (Gilbertson et al. 1987, Becker 1989, 1991, Furness 1993, Barrett et al. 1996, Becker et al. 1998, ICES 1999) and is implemented already in some current monitoring programmes in the North Sea. Monitoring of pollutants in seabirds is highly desirable as a cost-effective and informative procedure indicating change in marine contamination.

Advantages in the use of seabirds as indicators of organochlorine pollution have recently been reviewed (ICES 1999) and include the following features of seabirds: well-known taxonomy and biology, tendency to accumulate high concentrations, ease of sampling (eggs), known foraging range and diets, resistance to toxic effects, low variance of pollutant levels within the population. Consequently, seabirds offer some advantages compared to physical or other marine biotic samples when organochlorine monitoring is needed.

3.2.3.2 Robustness of proposed EcoQO

Levels of organochlorines in seabirds show an immediate response to changes in contaminant loads in the marine environment; consequently they clearly indicate changing levels (e.g., Thyen and Becker 2000) and reflect changes in anthropogenic discharges and emissions of organochlorines. In this way, the effectiveness of measures of reduction of contamination can be demonstrated. Trend data are available for various parts of the North Sea for nearly 40 years.

OSPAR (1997) has published guidelines for sampling and analysing (using gas chromatography) seabird eggs. The key compounds are PCBs, DDT and metabolites, HCB and HCH isomers, which can be analysed synchronously using the same analytical procedure. There is a clear parameter signal, as eggs can only be taken in the breeding season, thus reducing the effects of seasonal variation. The objective is relevant to the North Sea, where organochlorine inputs remain high (De Jong et al. 1999). Monitoring can investigate temporal and spatial variation as well as local contaminant input, as seabirds forage in restricted distances from colonies during the period of egg formation. Foraging ranges vary between species, but are generally well known. Studies in the southern North Sea show clear local differences in contamination between colonies. In the Wadden Sea, the common tern and the Eurasian oystercatcher were chosen in 1996 as monitoring species for organochlorines in the international Trilateral Monitoring and Assessment Programme.

3.2.3.3 Discussion

Current programmes demonstrate clearly the value of seabird eggs to indicate spatial and temporal trends in marine pollution with organochlorines (Becker et al. 1998, Thyen and Becker 2000). In the southern North Sea there has been a decreasing trend in organochlorine levels in seabird eggs since the early 1990s (Figure 3.6), but locally there are high levels (Figure 3.7) which, however, do not seem to be harmful to the birds during reproduction.

Sampling of seabird eggs as a means of monitoring seabird contamination with organochlorines should be developed into integrated marine pollution monitoring programmes, with the selection of appropriate locally common and internationally widespread monitoring species. A proposed list of species to be used for monitoring in the North Sea is given (Table 3.1). In addition to the organochlorines, some other relevant contaminants such as mercury can be analysed using the same samples.

Figure 3.6. Temporal trends in PCB contamination of Eurasian oystercatcher and common tern eggs from selected breeding sites of the Wadden Sea (TMAP). FW=fresh weight of egg content (Thyen and Becker (2000).

Figure 3.7. Spatial variation in organochlorine contamination of common tern eggs in 1996 and 1997 from breeding sites of the Wadden Sea (TMAP). Mean concentrations (ng g-1 egg fresh mass) and 95% confidence intervals are presented. N= 10 eggs each. From Becker et al. 1998.

3.2.3.4 Provisional estimates for EcoQOs in the North Sea

Reference level: 0 ng g-1 egg fresh mass. Levels are zero as these are man-made chemicals only produced during the past century.

Current levels (ng g-1 egg fresh mass, Southern North Sea, range of 6–7 sampling sites, data from 1997, Becker et al. 1998; CT = common tern; EO = Eurasian oystercatcher):

PCBs: CT 702 – 2042 (ng g-1 egg fresh mass); EO 492 – 1055 (ng g-1 egg fresh mass gg) DDT and metabolites: 56 – 371 (ng g-1 egg fresh mass); EO 22 – 103 (ng g-1 egg fresh mass) HCB: CT 11 – 325 (ng g-1 egg fresh mass); EO 4 – 60 (ng g-1 egg fresh mass) HCH: CT 5–15 (ng g-1 egg fresh mass); EO 3 – 10 (ng g-1 egg fresh mass)

Target levels: 0 ng g-1 egg fresh mass, but presumably this target could not be achieved until some decades from now as these persistent chemicals have long half-times.

Table 3.1. Seabird species suggested as monitors of marine pollution by organochlorines and mercury in the North Sea. Information on population size and trend, clutch size, diets and feeding range is presented (ICES 1999). Common tern and Eurasian oystercatcher are already in use for monitoring in the Wadden Sea TMAP.

Species Population size Trend Clutch Feeding range Diet size

Northern fulmar 307,600 pairs ++ 1 wide-ranging pelagic zooplankton, offal, discards, fish, squid Northern gannet 43,800 pairs ++ 1 wide-ranging sandeel, sprat, herring, mackerel, discards European shag 20,000 pairs = 3–4 rocky coastal sandeel, sprat Black-legged 415,500 pairs +/= 2 wide ranging small fish, zooplankton kittiwake Common tern 61,500 pairs +/= 2–3 coastal small fish Common guillemot 340,000 pairs + 1 inshore/offshore fish, especially sandeel, sprat Eurasian ? +? 3–4 coastal, intertidal areas shellfish, intertidal and terrestrial oystercatcher invertebrates

3.2.3.5 References

Barrett, R. T., Skaare, J. U. and Gabrielsen, G. W. 1996. Recent changes in levels of persistent organochlorines and mercury in eggs of seabirds from the Barents Sea. Environmental Pollution 92: 13–18.

Becker, P. H. 1989. Seabirds as monitor organisms of contaminants along the German North Sea Coast. Helgoländer Meeresunters 43: 395–403.

Becker, P. H. 1991. Population and contamination studies in coastal birds: the common tern Sterna hirundo. In: Perrins, C. M., J. D. Lebreton and G. J. M. Hirons. Bird population studies: relevance to conservation and management. pp. 433–460. Oxford University Press, Oxford.

Becker, P. H., Schumann, S. and Koepff, C. 1993. Hatching failure in common terns (Sterna hirundo) in relation to environmental chemicals. Environmental Pollution 79: 207–213.

Becker, P. H., Thyen, S. Mickstein, S., Sommer, U. and Schmieder, K. R. 1998. Monitoring pollutants in coastal bird eggs in the Wadden Sea. Final Report of the Pilot Study 1996–1997/Wadden Sea Ecosystem 8. Common Wadden Sea Secretariat Wilhelmshaven: 59–101.

De Jong, F., Bakker, J., van Berkel, C., Dahl, K., Dankers, N., Gätje, C., Marencic, H. and Potel, P. 1999. 1999 Wadden Sea quality status report. Wadden Sea Ecosystem 9, Common Wadden Sea Secretariat, Wilhelmshaven.

Elliott, J. E., Noble, D. G., Norstrom, R. J., Whitehead, P. E., Simon, M., Pearce, P. A. and Peakall, D. B. 1992. Patterns and trends of organic contaminants in Canadian seabird eggs, 1968–90. In: Walker, C. H. and Livingstone, D. R.. Persistent pollutants in marine ecosystems. pp. 181–194. Pergamon Press, Oxford.

Furness, R. W. 1993. Birds as monitors of pollutants. In: Furness, R. W. and Greenwood, J. J. D. Birds as monitors of environmental change. pp. 86–143. Chapman and Hall, London.

Gilbertson, M., Elliott, J. E. and Peakall, D. B. 1987. Seabirds as indicators of marine pollution. In: Diamond, A. W. and Filion, F. L. The value of birds. pp. 231–248. ICBP Technical Publication

ICES. 1999. Report of the Working Group on Seabird Ecology. ICES CM 1999/C:5

OSPAR. 1997. JAMP guidelines for monitoring contaminants in biota. 9/6/97, OSPAR Commission, London.

Thyen, S. and Becker, P. H. 2000. Aktuelle Ergebnisse des Schadstoffmonitorings mit Küstenvögeln im Wattenmeer. Vogelwelt 121: 281–291.

3.2.4 Eutrophication

Shorebird and gull numbers and density are affected by the nutrient status of the inter-tidal area on which they forage. Thus mudflats and estuarine systems that are moderately sewage-enriched attract higher numbers of birds prior to a clean-up than afterwards (van Impe 1985, Furness et al. 1986, Goss-Custard et al. 1991, Raven and Coulson 2001). Despite this, the Working Group could not think of a good example where seabirds would provide a more suitable way of monitoring eutrophication than direct measurement of the mudflat condition or investigation of invertebrates in the sediment. Effects of eutrophication on nearshore and offshore seabirds are not well known.

Furness, R. W., Galbraith, H., Gibson, I. P. and Metcalfe, N.B. 1986. Recent changes in numbers of waders on the Clyde Estuary and their significance for conservation. Proceedings of the Royal Society of Edinburgh, Series B 90: 171–184.

Goss-Custard, J. D., Warwick, R. M., Kirby, R., McGrorty, S., Clarke, R. T., Pearson, B., Rispin, W. E., le V. dit Durell, S. E. A. and Rose, R. J. 1991. Towards predicting wading bird densities from predicted prey densities in a post- barrage Severn estuary. Journal of Applied Ecology 28: 1004–1026.

Raven, S. J. and Coulson, J. C. 2001. Effects of cleaning a tidal river of sewage on gull numbers: a before-and-after study of the River Tyne, northeast England. Bird Study 48: 48–58. van Impe, J. 1985. Estuarine pollution as a probable cause of increase of estuarine birds. Marine Pollution Bulletin 16: 271–276.

3.2.5 Litter - Plastic particles

EcoQO title: An index of plastic particle pollution of the North Sea

3.2.5.1 Background

Seabirds ingest plastic particles floating in the seas and oceans, presumably confusing these with food (Furness 1985a, 1985b, van Franeker 1985, Ryan 1987, 1988). Some kinds of seabirds regurgitate pellets of indigestible stomach contents, so lose these plastic pellets. However, certain kinds of seabirds, especially Procellariiformes, accumulate these fragments of plastic in their stomach (gizzard) and retain them for many months or years (Ryan and Jackson 1987, Ryan 1988). Procellariiformes have a constriction between the proventriculus and gizzard that makes it very unlikely that plastic reaching the gizzard will be regurgitated (Furness 1985b). Over many months plastic fragments become abraded to a size that will eventually pass out of the gizzard into the intestine and will be voided in the faeces. Large quantities of plastic retained in the gizzard can reduce the ability of a bird to process food, and so can lead to a deterioration in body condition, although it is not easy to demonstrate this from field studies that correlate plastic load with body condition or mass (Furness 1985b, Ryan 1987, Spear et al. 1995). This may be due to death of birds that suffer

deterioration in body condition, but this has not been demonstrated by experiment or field study. In addition to the effect on stomach function, plastic particles adsorb toxic chemicals such as PCBs (Ryan et al. 1988, Mato et al. 2001) and so their ingestion by seabirds will tend to elevate burdens of these chemicals in the birds. Plastic particles in the oceans are both the industrial raw material (plastic pellets) and fragments of broken used plastic items. Seabirds will ingest both types, with some evidence for selection according to colour (Blight and Burger 1997, Moser and Lee 1992). Studies show that seabirds in all the world’s oceans contain plastic particles. In the North Sea, the only abundant Procellariiform seabird is the northern fulmar, so this species would be the one to sample to measure plastic burden. It is known to ingest plastic (Furness 1985a, van Franeker 1985, Camphuysen and van Franeker 1997).

3.2.5.2 Robustness of proposed EcoQO

Numbers of plastic particles per bird vary enormously between individuals within a population, so that moderately large sample sizes (ca 40 individuals) are required to provide a small standard error of the mean to permit trends to be measured over time or between regions. Most studies of plastic loads in seabirds have used samples of seabirds found dead or collected for other purposes, so that bias in sampling may affect results (for example, birds found dead on beaches tend to include high proportions of juvenile birds which may have less plastic than found in mature birds). This is not necessarily a major limitation, since birds can be classified by age group and other criteria to reduce or eliminate this potential bias. There is evidence of an increase in amounts of plastic in seabirds from a long-term (14 year) study of western North Atlantic seabirds (Moser and Lee 1992), from studies in other oceans (Robards et al. 1995) and from comparisons of samples of particular species collected in the same region in different years/decades. If the plastic burden was so high that it caused a significant increase in mortality of birds with large burdens then sampling could overestimate plastic pollution if birds found dead on beaches were sampled (these would over-represent individuals with high loads of plastic), whereas it could underestimate plastic pollution if breeding birds were killed as a sample (these would not contain birds in poor condition due to plastic as such birds would be unlikely to breed due to poor condition).

Sampling of northern fulmars could be done by collecting fresh corpses from beaches around the North Sea, as this would provide large sample sizes and classification of these birds into age classes would quantify differences related to age group. Northern fulmar is one of the more commonly found dead birds on North Sea beaches. It would not be ethically acceptable to kill healthy birds to assess plastic loads on a regular basis, but samples of birds killed by accident (e.g., through long-line by-catch mortality) might be useful to calibrate bias in plastic loads of birds found dead compared to birds sampled alive. The northern fulmar is the most frequently caught bird in the Norwegian long-line fishery in the northern North Sea and Norwegian Sea.

3.2.5.3 Discussion

Given that the harmful effects of ingested plastic in seabirds have been established as affecting body condition and increasing uptake of several toxic chemicals, and given that plastic particle pollution is generally increasing in the world’s oceans, this EcoQO should be given a high priority, despite the fact that our present knowledge of plastic particle burdens of northern fulmars in the North Sea is rather limited.

3.2.5.4 Provisional estimates for EcoQOs in the North Sea

Numbers of plastic particles in gizzards of northern fulmars classified by age group and cause of death

Reference level: 0%

Since plastics are not naturally occurring, all plastic found in seabird stomachs is due to human activity.

Current level:

Not accurately known. Northern fulmars were sampled in the early 1970s and early 1980s. At Shetland, 13 breeding adult birds had a mean of 10.6 plastic particles with a maximum of 40, in the early 1980s (Furness 1985a). On the coast of The Netherlands 65 birds found dead on beaches had a mean of 11.9 plastic particles with a maximum of 96, also for birds sampled in the early 1980s (van Franeker 1985). However Bourne (in van Franeker 1985) found only 1–2 plastic particles per bird in fulmars examined in the early 1970s. Given the apparent increase in plastic particle pollution in oceans and seas worldwide, and likely adverse effects on seabirds, the current level in fulmars should be established as a matter of high priority.

Target level:

Since all plastic is anthropogenic, the target should be as low a level as possible. For practical reasons it cannot be set at zero, since such a low target would be unrealistic. Study of the lowest amount that influences body condition or significantly increases the uptake of toxic chemicals is required to provide the means to set a target at a level somewhat below the lowest amount found to cause harm to seabirds. In the absence of such data at present, a provisional target level can be suggested as follows. Studies detecting effects on body condition of seabirds reported loads of around 10– 100 plastic particles in the most contaminated individual birds. Thus the target should be clearly less than that range. We suggest that until data are available on the amount of plastic that affects northern fulmar body condition or contaminant uptake, a target should be set at a maximum of no more than 10 plastic particles in any individual within a sample of at least 40 northern fulmars. This would represent a considerable reduction from levels found during the early 1980s, and so probably an even larger reduction from present-day levels.

3.2.5.5 References

Blight, L. K. and Burger, A. E. 1997. Occurrence of plastic particles in seabirds from the eastern North Pacific. Marine Pollution Bulletin 34: 323–325.

Camphuysen, C. J. and van Franeker, J. A. 1997. Notes on the diet of northern fulmars from Bjørnøya. Sula 11: 1–10.

Furness, R. W. 1985a. Plastic particle pollution – accumulation by Procellariiform seabirds at Scottish colonies. Marine Pollution Bulletin 16: 103–106.

Furness, R. W. 1985b. Ingestion of plastic particles by seabirds at Gough Island, South Atlantic Ocean. Environmental Pollution 38: 261–272.

Mato, Y., Isobe, T., Takada, H., Kanehiro, H., Ohtake, C. and Kaminuma, T. 2001. Plastic resin pellets as a transport medium for toxic chemicals in the marine environment. Environmental Science and Technology 35: 318–324.

Moser, M. L. and Lee, D. S. 1992. A 14-year survey of plastic ingestion by western North-Atlantic seabirds. Colonial Waterbirds 15: 83–94.

Robards, M. D., Piatt, J. F. and Wohl, K. D. 1995. Increasing frequency of plastic particles ingested by seabirds in the sub-Arctic North Pacific. Marine Pollution Bulletin 30: 151–157.

Ryan, P. G. 1987. The effects of ingested plastic on seabirds – correlations between plastic load and body condition. Environmental Pollution 46: 119–125.

Ryan, P. G. 1988. Intraspecific variation in plastic ingestion by seabirds and the flux of plastic through seabird populations. Condor 90: 446–452.

Ryan, P. G. and Jackson, S. 1987. The lifespan of ingested plastic particles in seabirds and their effect on digestive efficiency. Marine Pollution Bulletin 18: 217–219.

Ryan, P. G., Connell, A. D. and Gardner, B. D. 1988. Plastic ingestion and PCBs in seabirds – is there a relationship. Marine Pollution Bulletin 19: 174–176.

Spear, L. B., Ainley, D. G. and Ribic, C. A. 1995. Incidence of plastic in seabirds from the tropical Pacific, 1984–91 – relation with distribution of species, sex, age, season, year and body-weight. Marine Environmental Research 40: 123– 146. van Franeker, J. A. 1985. Plastic ingestion in the North Atlantic fulmar. Marine Pollution Bulletin 16: 367–369.

3.3 Fisheries

3.3.1 By-catch of seabirds

In some oceans, by-catch of seabirds in fishing gear is a major factor affecting seabird populations. In particular, long- lines have had a measurable and great impact on some albatross and petrel populations, and gill-nets have affected populations of seabirds that dive for fish. Surveys in the North Sea have shown that seabird by-catch in fishing gear is probably relatively localised and sporadic (Oldén et al. 1988, Robins, 1991, Murray et al. 1994). On this basis, we consider that it would be difficult to set a quantifiable and meaningful EcoQO, but would wish to see any such by-catch minimised.

3.3.1.1 References

Murray, S. Wanless, S. and Harris, M. P. 1994. The effects of fixed salmon Salmo salar nets on guillemot Uria aalge and razorbill Alca torda in northeast Scotland in 1992. Biological Conservation 70: 251–256.

Oldén, B., Peterz, M. and Kollberg, B. 1988. Sjöfågeldöd i fisknät i nordvästra Skåne. Naturvårdsverket Rapport 3414. Solna, Sweden. 51pp.

Robins, M. 1991. Synthetic gill nets and seabirds. Royal Society for the Protection of Birds/World Wide Fund for Nature, Sandy, UK.

3.3.2 Harvesting of seabird food

EcoQO title: An index of breeding productivity of black-legged kittiwake as an index for sandeel stocks in the North Sea

3.3.2.1 Background

Sandeels are among the most abundant fish in the North Sea and dominate the summer diets of many marine vertebrates (Furness and Tasker 1997), especially in the north-west of the region where there are few sprat or juvenile herring to provide alternative prey. Sandeel therefore represent an important component of ecological quality in the North Sea. A large industrial fishery also harvests sandeels and there is potential for this to reduce ecological quality through localised over-exploitation (Furness 1999a, 1999b). Stocks of sandeel are extremely difficult to assess owing to fluctuations in recruitment, their high, variable natural mortality rate and their burrowing behaviour (Gislason and Kirkegaard 1996). At present sandeel stocks are estimated at a broad spatial scale (Gislason and Kirkegaard 1996) despite evidence for finer-scale population structure (Pedersen et al. in press). Regional stock assessments are therefore desirable, particularly in environmentally sensitive areas that occur at smaller spatial scales (Furness and Tasker 2000). An EcoQO that provides both a recognition of biological impact and a surrogate measure of local declines in sandeel stocks has clear value for ecologically sensitive fisheries management.

3.3.2.2 Robustness of the proposed EcoQO

The productivity of black-legged kittiwakes has the potential to provide such an EcoQO for sandeel fisheries, with variations in productivity indicating changes in the ecological quality of the sandeel stock and dependent predators. The productivity of black-legged kittiwakes is more sensitive than that of most other seabird species to changes in prey availability due to their relatively small size, short foraging range, surface-feeding habits and limited scope to increase foraging effort (Furness and Tasker 2000). In the north-west North Sea, kittiwakes are largely dependent on sandeel for food owing to the low availability of alternative small, schooling fish. Black-legged kittiwake productivity is correlated with sandeel abundance in the North Sea and in Shetland (Furness 1999a) and variation due to other factors such as predation and storms can generally be recognised and controlled. Changes in black-legged kittiwake productivity and sandeel abundance occur within a single summer and so provide an immediate annual index of sandeel abundance (Furness 1999a). Productivity is easy to measure and a time series of data is available from most of their North Sea breeding range to provide current levels of the EcoQO (Upton et al. 2000). Monitoring will continue in the future according to an agreed protocol. Black-legged kittiwake breeding distribution in the North Sea is largely confined to north-east England and Scotland (Lloyd et al. 1991) owing to their dependence on cliffs for nesting habitat. They have a limited foraging radius that is generally within 50 km of their colony (Furness and Tasker 2000), and so the EcoQO is confined to the north-west North Sea. There is limited spatial overlap of sandeel fishing and black-legged kittiwake

foraging areas during the breeding season as most fishing effort is directed at offshore sandbanks (Wright and Begg 1997, Furness and Tasker 2000).

3.3.2.3 Discussion

Black-legged kittiwake productivity has the potential to provide a reasonably robust EcoQO for sandeel stocks that have a great significance as a component of the marine food web and are difficult to quantify by conventional means. The limited geographic scope of the EcoQO owing to constraints of black-legged kittiwake nesting habitat and foraging ranges does reduce its value over the North Sea as a whole. However, black-legged kittiwake productivity provides a valuable EcoQO for fisheries operating inshore near seabird colonies such as Wee Bankie and Shetland. These are areas where ecologically sensitive management of sandeels is important, and kittiwake productivity provides a valuable tool to inform stock management as well as an indicator of ecological quality.

3.3.2.4 Provisional estimates for EcoQOs in the North Sea

Reference Level: No information concerning levels of regional sandeel stocks and the levels of kittiwake productivity that these supported in the absence of anthropogenic influence is available. Reductions in fish predators such as mackerel and gadoids in the North Sea (that are even now the major consumers of sandeel; Furness and Tasker 1997) have had large influences on sandeel availability and their stock levels prior to this occurring are unknown. Therefore no quantitative reference level can be presented.

Current Level: The current level of productivity in the north-west North Sea is 0.97 ± 0.28 chicks per pair, based on colonies in the north-west North Sea from 1986–1996, but excluding Shetland where predation by great skuas and atypically low sandeel availability has reduced breeding success (Furness 1999b).

Target Level: The target level for black-legged kittiwake productivity is a minimum of 0.5 chicks per pair. The EcoQO would not be met if productivity fell below this level. This is a level that was judged to reflect a favourable ecological quality of sandeel.

3.3.2.5 References

Furness, R. W. 1999a. Does harvesting a million metric tonnes of sand lance per year from the North Sea threaten seabird populations? Pp. 407–424 In: Ecosystem Approaches for Fisheries Management, Alaska Sea Grant College Program, AK-SG-99–01, Fairbanks.

Furness, R. W. 1999b. Are industrial fisheries a threat to seabird populations. Proceedings of the International Ornithological Congress, Durban.

Furness, R. W. and Tasker, M. L. 1997. Seabird consumption in sandlance MSVPA models for the North Sea and the impact of of inductrial fishing on seabird population dynamics. Pp. 147–169 In: Proceedings Forage Fishes in Marine Ecosystems, Alaska Sea Grant College Program, Fairbank.

Furness, R. W. and Tasker, M. L. 2000. Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance, and identification of key areas for sensitive seabirds in the North Sea. Marine Ecology Progress Series 202, 253–264.

Gislason, H. and Kirkegaard, E. 1996. The industrial fishery and North Sea sandeel stock. Seminar on the Precautionary Approach to Ecosystem Management, Oslo, 9–10 September 1996.

Lloyd, C., Tasker, M. L. and Partridge, K. 1991. The status of seabirds in Britain and Ireland. Poyser, London.

Pedersen, S.A. Lewy, P. and Wright, P.J. in press. Assessments of lesser sandeel (Ammodytes marinus) in the North Sea based on revised stock divisions. Fisheries Research.

Upton, A.J. Pickerell, G. and Heubeck, M. 2000. Seabird numbers and breeding success in Britain and Ireland. JNCC, Peterborough.

Wright, P. J. and Begg, G. 1997. A spatial comparison of common guillemots and sandeels in Scottish waters. ICES Journal of Marine Science 54: 578–592.

3.3.3 Increase in seabird food supply

Fisheries in the North Sea generate large quantities of waste in the form of discarded fish and offal. Much of this waste is consumed by scavenging seabirds (Camphuysen et al. 1995, Garthe et al. 1996). Nearly all populations of scavenging seabirds have increased over the past century, probably due mainly to a relaxation in persecution coupled with this artificially increased food supply. Numbers of seabirds that feed by diving to catch small fish underwater have also increased over the period. In this case it seems likely that availability of forage fish stocks has increased through reduction in stock size, and thereby competition, of the larger predatory fish such as cod and mackerel. Many species of seabirds in the North Sea are thus at relatively high or peak levels historically.

In both cases outlined above, a corollary of better management of fish stocks and fisheries in the North Sea, through for instance the avoidance of capture of undersized or non-target fish or through reduction in overall fishing mortality, would be a likely decline in seabird population size. Such a decline in population size would be very difficult to predict (partly through likely unforeseen indirect community effects) and certainly should not be managed. It is thus very difficult to set either reference or target levels directly for seabird populations or as an index of improved management of fisheries for the main piscivorous predators in the North Sea.

3.3.3.1 References

Camphuysen, C. J., Calvo, B., Durinck, J., Ensor, K., Follestad, A., Furness, R. W., Garthe, S., Leaper, G., Skov, H., Tasker, M. L., and Winter, C. 1995. Consumption of discards by seabirds in the North Sea. Final Report to European Commission, study contract BIOECO/93/10, NIOZ Report 1995-5, Netherlands Institute for Sea Research, Texel. 202pp.

Garthe, S., Camphuysen, C. J. and Furness, R. W. 1996. Amounts of discards in commercial fisheries and their significance as food for seabirds in the North Sea. Marine Ecology Progress Series 136: 1-11.

3.3.4 Mariculture

As noted in Section 5 of this report, seabirds interact with mariculture. The scale of this interaction appears to be comparatively small in ecosystem terms so birds are probably not a good indicator of the impact of marine farms on the ecosystem. There are some areas where marine farming operations may be having an affect on bird populations; if this effect is negative and large enough, then the monitoring that is required for seabird population EcoQO (Section 3.4.1) will detect it.

3.4 Habitats and ecosystem health

3.4.1 Seabird populations

EcoQO title: Seabird population trends as an index of seabird community health in the North Sea

3.4.1.1 Background

At North Sea latitudes environmental variability is expected to be relatively large and, hence, at any one time most seabird populations will be either increasing or decreasing in numbers. Consequently, healthy seabird communities in the North Sea are also characterised by significant population changes within limits set by natural factors. Documented changes in seabird populations cannot usually be explained in full due to a lack of information on how various natural and human-induced environmental factors affect their main population parameters such as reproduction, recruitment and survival rates. Obviously, there is no need to initiate intensive research aimed at explaining all changes in seabird numbers. The magnitude of such changes may, nevertheless, serve as an adequate EcoQO for the intrinsic health of seabird communities. This is based on the simple assumption that a pronounced negative trend in the population of any seabird species could indicate that it is an undesirable effect of human activities. In other words, when a certain level of population change is reached, the public concern is regarded to be so great that it represents a provisional reduction of ecological quality. Ideally, and as a precautionary measure, reaching such a threshold should then trigger adequate studies targeted at revealing its underlying causes. If the change proves to be an undesired consequence of human activities, any useful mitigating measures should be identified and implemented. In some cases, monitoring the effect of these measures may benefit from defining additional and more specific EcoQOs for the seabird populations and/or environmental factors involved.

3.4.1.2 Robustness of proposed EcoQO

On a short-term scale, seabird population size is not the parameter most sensitive to environmental change. Due to the longevity and delayed maturity of most seabirds, several years are usually needed before changes in their reproduction or immature survival rates affect their breeding numbers. Nevertheless, changes in population sizes are reasonably good indicators of important changes in seabird community structure, where density-dependent effects may easily reduce the usability of other population parameters. Furthermore, population size of breeding birds and birds wintering in coastal areas is far easier to monitor extensively throughout the geographic range of the target populations

3.4.1.3 Provisional estimates for EcoQOs in the North Sea

Population trends of seabirds in the North Sea

Reference levels: Variable, but largely of unknown magnitude

Current levels: Variable, see Section 2

Target level: ≤ 20 % decline over ≥ 20 years (more details below)

Setting a target level for a population change that deserves extra attention in this context is no straightforward task. However, we believe the criteria used to identify bird species of European conservation concern based on the definition of a moderate decline (Tucker and Heath 1994) is useful for this EcoQO. This would mean that a reduction in the population of a seabird species deserves special attention if it has, over a period of less than 20 years, declined in size or range by at least 20% in 33–65% of the population or by at least 50% in at least 25% of the population. This criterion has been proposed to the OSPAR Biodiversity Committee for use in other parts of the NE Atlantic. Assessed on the background of the known trends for seabird populations in the North Sea (Chapter 2), WGSE finds that this suggestion sets a reasonable target level for the proposed EcoQO. It is not very different from the target level suggested by Anker- Nilssen et al. (1996) to identify the need for more detailed studies or management actions, although they argued that also positive trends of similar magnitude deserve attention. In such cases, we recommend that the attention is primarily addressed to explain increases in species that could conflict with other seabird populations that are falling under the target level.

3.4.1.4 References

Anker-Nilssen, T., Erikstad, K. E. and Lorentsen, S.-H. 1996. Aims and effort in seabird monitoring: an assessment based on Norwegian data. Wildlife Biology 2: 17–26.

Tucker, G. M. and Heath, M. F. 1994. Birds in Europe. Their conservation status. BirdLife International, Cambridge.

3.4.2 Threatened and declining seabird species in the North Sea

EcoQOs for threatened and declining species in the North Sea other than seabirds are being developed by another working group (Gubbay 2001). WGSE felt that those seabirds that were threatened or declining should be considered for EcoQOs to maintain consistency across taxa. Gubbay (2001) has devised criteria based on international conservation threat listings, importance of the North Sea for their populations and a status that was threatened by anthropogenic factors relevant to OSPAR’s management remit. We followed these guidelines to determine whether any seabird species warranted EcoQOs.

The conservation status of seabirds in Europe was determined using Tucker and Heath (1994). We classed species as being threatened or declining if they were listed as endangered, vulnerable, rare or declining that were concentrated in Europe (but not if this is solely due to localised distribution). Furthermore, we only included those seabird species with over 50% of the European population occurring in the North Sea. Only species that are declining in the North Sea due to anthropogenic activities that fall within OSPAR’s remit to manage (pollution) were included to ensure that any resultant EcoQOs were relevant to the target audience.

No seabird species in the North Sea met all of these criteria and we therefore believe that an EcoQO for any single seabird species occurring in the North Sea is not appropriate.

3.4.2.1 References

Gubbay, S. 2001. Development of ecological quality objectives for the North Sea: threatened and declining species. Report to BirdLife International, Sandy. 41p.

Tucker, G. M. and Heath, M. F. 1994. Birds in Europe. their conservation status. Birdlife International, Cambridge.

3.5 Hunting/harvesting

There is little if any hunting of breeding seabirds currently in the North Sea, but this pressure on seabird populations was very large in the past and declined steadily through the 20th century. Wintering seaducks and wading birds are still hunted under licence for sport and food. The scale of such hunting is not believed to be large in relation to North Sea populations, though it may be detectable locally. The licensing schemes for hunters should be managing this impact to sustainable levels. Many hunting schemes include features such as emergency closure during periods of extreme weather when the disturbance caused by hunting would cause an undue adverse effect on populations. WGSE does not believe that an EcoQO would add to the ability to manage sustainable hunting in the North Sea.

3.6 Disturbance

Human recreational usage of the North Sea and its coasts is intensive. In some areas, disturbance from such recreation is sufficient to reduce habitat available for use by seabirds. This habitat can be feeding, resting and breeding grounds. It is likely that such loss of available habitat has depressed the overall numbers of birds using the North Sea. Examples include loss of breeding areas on beaches for Kentish plover and little tern and loss of estuarine feeding areas for shorebirds and waterbirds. It is however difficult to distinguish the signal coming from such disturbance from the number of other factors affecting seabirds, so although EcoQOs could be set as targets for management of the individual species, WGSE felt that this would not be useful in managing for reduction in disturbance.

3.7 Introduced/conflicting species

Most oceanic birds are relatively defenceless against mammalian predators and for this reason most seabird colonies are located on offshore islands or on inaccessible cliffs that have no populations of mammals. Subsequent introductions, intentional or otherwise, of mammals to islands have had disastrous consequences for seabirds (Folkestad 1982, Knight and Haddon 1982, Southern et al. 1982, 1985, Steiniger 1956). Chicks, eggs and some adults of some alcids and terns are taken by gulls and skuas in the North Sea area, and incidental predation by other birds such as common ravens has been recorded but these instances of predation seem to be of minor consequence to the populations of North Sea seabirds.

In the North Sea area, the species of mammals that have had most significant impact upon seabirds are brown rats, feral cats, American mink, fox and hedgehog. American mink that have caused damage are escapes from commercial fur farms. Such farms have been banned from Shetland and Orkney, but still operate in other parts of Scotland. Hedgehogs have been deliberately introduced to some islands off Scotland. Brown rats and feral cats have spread to wherever man has been resident for any time.

There are numerous instances worldwide in which insular populations of seabirds have been extirpated by predation from introduced mammals. One example (and there are many more) is Isle aux Cochons in the Crozet Islands of the Indian Ocean. On this island, introduced and now feral cats have probably been responsible for the extirpation of ten species of seabirds, and it has been estimated that feral cats are responsible for consuming 1.2 million seabirds there per year (Pascal 1980, Moors and Atkinson 1984). All species of gulls nesting around the North Sea have been impacted by predation from American mink and red fox. Brown rats have been implicated in reductions of Manx shearwater and European storm-petrel populations in the UK, and American mink, red fox, and hedgehogs have taken eggs, chicks and adults of gulls and terns. Rats, cats and foxes have depredated terns and gull colonies in the Wadden Sea.

There has been some recent success in ridding North Sea seabird islands of mammalian predators, though the job is labour intensive and time consuming (Moors and Atkinson 1984). The only North Sea species in danger of local extinction due to predation by mammals is the roseate tern, and strict measures are being taken to prevent access by mammals to the nesting islands. WGSE considered that an EcoQO using seabirds to indicate the state of islands in relation to introduced mammals would not improve on surveying for the introduced mammals directly. An index of numbers of islands without introduced mammals could be derived and could be used as an index of progress in ridding islands of introduced and invasive species.

3.7.1 References

Folkestad, A. D. 1982. The effect of mink predation on some breeding seabird species. Viltrapport 21: 32–34.

Knight, R. C. and Haddon, P. C. 1982. Little terns (Sterna albifrons) in England and Wales 1977–79, with details of conservation work carried out at Rye Harbour local nature reserve. Seabird Report 6: 70–85.

Moors, P. J. and Atkinson, I. A. E. 1984. Predation on seabirds by introduced animals and factors affecting its severity. Pages 667–690 in Croxall, J. P., Evans, P. G. H. and Schreiber, R. W. (Eds) Status and Conservation of the World’s Seabirds. International Council for Bird Preservation, Cambridge. Technical Publication No. 2.

Pascal, M. 1980. Structure et dynamique de la population de chats harets de l’archipel des Kerguelen. Mammalia 44: 161–182.

Southern, L. K., Patton, S. R., and Southern W. E. 1982. Nocturnal predation on Larus gulls. Colonial Waterbirds 5: 169–172.

Southern, W. E., Patton, S., Southern, L. K. and Hanners, L. A. 1985. Effects of nine years of fox predation on two species of breeding gulls. Auk 102: 827–833.

Steiniger, F. 1956. Uber die Wanderratte auf den deutschen Nordseeinseln. Beitrage Naturkunde Niedersachsen 9: 3– 10.

Upton, A. J. Pickerell, G. and Heubeck, M. 2000. Seabird numbers and breeding success in Britain and Ireland. JNCC, Peterborough.

3.8 Climate change

Given that the linkages between climate change and seabird dynamics are mainly through several lower trophic levels, and that seabirds have quite robust mechanisms to buffer themselves against such perturbations, it is unlikely that seabirds would provide a strong EcoQO in relation to impacts of climate change. The most likely responses of seabirds to climate change will probably be modulated through effects of changes in food fish distributions and abundance.

4 FURTHER DEVELOPMENT OF SEABIRD MONITORING

4.1 Introduction

As long-lived top predators foraging over long distances at sea, seabirds can integrate marine environmental conditions over wide spatial and temporal scales, and respond with changes of life history parameters to various fluctuations in the marine environment. Aspects of their breeding and feeding ecology reflect seasonal and inter-annual changes in the productivity of oceans (Anderson et al. 1982, Cairns 1987, Croxall et al. 1988, Furness and Nettleship 1990). Because some seabirds feed on commercial species, their monitoring should provide information on the status of prey stocks, for instance when there is a large drop in the stocks (Montevecchi and Berruti 1990). Furthermore, parameters of reproductive performance of seabirds may be indicators at meso or macro scale (Hunt and Schneider 1987) of short and long-term changes in oceanographic conditions (Boersma 1978, Schreiber and Schreiber 1984, Croxall et al. 1988). Certain oceanographic anomalies may be so significant that they can be quickly detected at the upper food level. In addition, various species of seabirds may have the potential to reflect large-scale oceanographic anomalies in their breeding, although their life history parameters may respond differently. Long-term studies in North Sea provided evidence that demographic parameters of seabirds may be correlated with changes in physical factors (Aebisher et al. 1990). Several of these parameters such as population size, breeding success, duration of foraging trips, changes in body mass, or chick growth rate, have shown to be responsive to changes in environmental conditions.

As top predators in the marine food webs, seabirds accumulate environmental contaminants that can easily be measured in eggs or feathers. Consequently, seabirds have been used as monitors of ocean pollution by heavy metals and xenobiotics (e.g., Furness 1993, Becker et al. 1998, ICES 1999) or by oil (Camphuysen and Heubeck 2001).

These characteristics qualify seabirds as biomonitors, and they are accepted and already in use as indicators of various aspects of the marine environment (e.g., Furness and Greenwood 1993, ICES 1999, 2000) either as sensitive indicators or as accumulative indicators of pollutants. They have become parts of national and international monitoring

programmes (see examples below). However their use as indicators of the marine environments could be further increased because of their value and advantages as biomonitors. By monitoring parameters additional to those presently used, and by establishing monitoring schemes at wider geographical and international scales, the value of seabirds as monitors of marine environmental change could be much improved.

In this chapter, we review a variety of parameters measured in seabirds and assess their usefulness as indicators of environmental quality and change to detect short-term and long-term ecosystem effects. In addition we make recommendations for designing monitoring programmes using seabirds.

4.2 Demands for the parameters and seabird species selected for monitoring

Main aims of marine monitoring with seabirds is to use them:

• as sensitive indicators of environmental change, by studying demographic parameters; • as indicators of food supply and availability, by studying diets and provisioning of young; • as accumulative indicators of marine pollution.

What are the preconditions of successful monitoring?

• The monitoring aims should be clearly defined: human effects on the marine ecosystem are the focus of interest, e.g., by fishing or by pollution with oil or environmental chemicals. • Sensitivity: The species and parameters selected should be sensitive to the specific change in the marine environment. • High signal to noise ratio: The response of the parameter to a specific environmental change should be distinct from sources of other variation (“noise”) and accessible to investigation by scientific methods. • Practicability: The parameters should be easy to measure; an advanced and accepted methodology should exist, described in guidelines; the monitoring should be cost effective (favourable, accessible sites, man power, costs for field work, data management and evaluation). • To be used as early warning of the environmental state, data evaluation has to be carried out continuously, that means by scientific staff.

Figure 4.1 Scheme of the most important parameters as a function of time scale integrating marine resource abundance and availability in seabirds.

The parameters of life history are indicative of potential changes at different temporal and spatial scales (Figure 4.1). Most of the breeding parameters integrate the environmental situation during the breeding season and the sea area around the breeding colonies, whereas survival rates and population size reflect environmental influences over the whole year, over breeding as well as migrating areas and with long-term consequences for the population.

The selected indicator species should be common and widespread to be able to cover various sea areas, prey stocks and to detect spatial trends within one species.

4.3 Seabirds as sensitive indicators for change in the marine environment: Monitoring characteristics of seabird life history besides population size

In general, seabirds are extreme long-lived species with high adult survival and low annual reproductive output. Many species delay first breeding until several years old. In consequence, the non-breeding proportion of the population is high.

Seabird numbers in a population change as a consequence of births, deaths, immigration and emigration. Much effort has been put into surveillance of the size of seabird populations, and almost all of this effort has been directed at the census or sample monitoring of breeding numbers. This is largely because it is much easier to make accurate counts of breeding birds, or nests, than it is to count all birds in seabird populations. However, changes in breeding numbers may reflect not only births, deaths, immigration and emigration, but also changes in age of recruitment (first breeding), changes in the proportion of mature birds that choose not to breed in a particular year (deferred breeding), or changes in timing or synchrony of breeding that can be confounded with changes in breeding numbers if, as is often the case, census counts of nests or breeders are made on a particular date in the breeding season.

Life history theory envisages trade-offs between components of fitness, such as survival and reproductive investment (Roff 1992, Stearns 1992, McNamara and Houston 1996), and leads us to anticipate that seabird breeding numbers (equivalent to estimated ‘population size’) may vary as a consequence of such trade offs by seabirds. Monitoring seabird breeding numbers alone, will not only fail to provide any indication as to the cause of a measured change in

numbers, but also may present a less than optimal approach to detecting change, since specific life history parameters may vary more strongly in response to changes in food supply than would breeding numbers (e.g., Cairns 1987). For example, breeding success may show strong relationships with food supply but despite this there may be little consequent impact on breeding numbers, as a result of various forms of buffering of breeding numbers. Even if this were not the case, changes would only be manifested some years later owing to deferred breeding. Also, while change in food abundance may affect breeding success, small and often undetected changes to adult survival might have a more significant influence on population change (ICES 2000).

Dynamic interactions between the life history traits exist (ICES 2000), underlining the necessity to look to many of the relevant population parameters to be able to find the causes for population changes and influences of changes in food supply or pollutants. In consequence, to use seabirds as indicators of change in the marine environments, other life history parameters should be selected in addition to population size.

In 2000 the Working Group briefly reviewed life history traits with respect to their desirability, feasibility and practicability as characteristics for monitoring seabird population dynamics is response to changes in food supply (ICES 2000, Table 1). Here we refer to the results of our review and address the population parameters that are important for population regulation and worth taking into consideration for future seabird monitoring.

Table 4.1. Monitoring of important life history parameters of seabirds. The most important parameters are emboldened.

Parameter Desirability Feasibility Practicability Population - population size (breeders) +++ +++ +++ - incidence of non-breeding + + - - adult survival +++ ++ + - subadult survival to breeding +++ ± - - recruitment % of fledglings ++ ± - % recruits in population + ± ± - recruitment age + + ± - immigration rate + - - - emigration rate + - - - sex ratio of the breeding population ± - - - age structure of the population ++ ± -

Reproduction and food provisioning - reproductive success ++ ++ ++ - laying date + ++ ++ - clutch size + +++ ++ - egg size + +++ ++ - chick growth rate + ++ + - mass of fledglings + ++ + - adult nest and brood attendance; ++ ++ ± provisioning rate - degree of kleptoparasitism + ++ ± -attendance of pre- and nonbreeders + ± ±

Body condition of breeders + + +

+++ highest; ++ high; + moderate; ± more or less; - low

4.3.1 Monitoring important life history parameters in seabirds

Table 4.1 presents the life history parameters most relevant for integrated population studies in seabirds. We distinguish between different degrees of desirability to measure a specific characteristic, of the feasibility and practicability to record it (financial and/or logistic reasons; man power). In this report we concentrate on the parameters of highest rates of desirability, feasibility and/or practicability, emboldened in Table 4.1.

4.3.2 Survival of adults and subadults

4.3.2.1 Adult survival

Sensitivity modelling reveals that among the demographic parameters adult survival and also subadult survival have the most decisive influence on population size in seabirds, but indicates also interspecific differences owing to various life history strategies (e.g., Croxall and Rothery 1991, ICES 2000).

To calculate adult survival, local recordings (resighting, retrapping) are necessary over many years. Very large samples are required to detect a significant change in the survival rate. For instance, in the wandering albatross for a sample of 1000 birds the standard error of an annual survival estimate, assuming a 100 per cent recapture rate, is 0.8 per cent per annum (Croxall and Rothery 1991). For such long-lived birds a consistent reduction in survival of 1–2 per cent per year can be highly significant for the population. Also accurate estimates of survival in one year cannot be made until a further 2 years have elapsed, because of the need to account for the probability of detecting individuals (Lebreton et al. 1992).

To use survival rates as parameter at a medium time scale its year-by-year calculation is necessary. This implies intensive annual recapture or resighting activities at the study site that is possible only in intensive integrated monitoring studies.

The use of ring recoveries to analyse survival requires many previous years of intensive ringing and large spatial scales, and only allows retrospective insight in survival over long time scales. Therefore, ringing recoveries cannot be used as indicator of recent changes in survival, which may be needed as an early warning of the health of the population or an important environmental change. Also, the estimates tend to be less precise and more biased than resightings.

4.3.2.2 Subadult survival to breeding

Estimation of juvenile survival also needs large samples of marked birds. In species with long-deferred sexual maturity there will be a considerable delay in obtaining results from live resighting studies.(e.g., Harris et al. 1992). For some species, this may be short-circuited by obtaining estimates of survival from the birds that attend the colony in the years prior to that of recruitment. Variation in the survival of subadults is much greater than in that of adults (ICES 2000).

A problem in estimating subadult survival is that, without very widespread monitoring, only local recruits can be covered. That means that local return rate is measured; the percentage of emigrated birds cannot be recorded. Another problem is that subadults normally cannot be recorded with high probability before they are breeders and it likely that there is a strong heterogenity in the probability of detecting individuals. Analysis of dead recoveries circumvents this, but other problems exist.

Recently, capture-mark-recapture models have been applied to estimate the proportion of individuals of different ages that have previously bred (e.g., Oro and Pradel 2000).

4.3.2.3 Recruitment to the breeding population

This parameter has also a high desirability, but even lower practicability than subadult survival. It can only be estimated in integrated population studies by resighting studies of marked birds recruiting to the natal colony. One innovative method to be able to monitor recruitment is marking birds with transponders and checking the breeding and non- breeding adults present at the colony site automatically year by year (Becker et al. 2001). The problem of measuring only natal colony recruitment remains an issue here.

4.3.3 Reproductive performance and success

Reproductive performance indicates the actual environmental situation at the breeding site and the adjacent sea areas during a respective year. For some species, productivity is not necessarily a very sensitive indicator of reproductive performance (Hunt et al. 1986) and may be influenced by factors other than food supply. These factors include predation, weather, flooding, pollution and disturbance (Becker 1998). Another limitation is that the indicative value of productivity is restricted mainly to the environmental situation during the reproductive period, excluding other periods of the year.

Estimation of breeding success of a population is usually very straightforward, requiring only estimates of the number of chicks fledging per pair. The extent to which breeding success reflects food abundance seems to vary among seabird species, and this variation is somewhat consistent. For example, northern fulmars and common guillemots tend to show about the same breeding success in all colonies under almost all conditions of food abundance, weather and other environmental variation. At the other extreme, breeding success of terns is highly variable among sites and years, being very severely affected by food abundance, but also by weather, disturbance, and predation (Becker 1998).

Further aspects of reproductive performance in seabirds may be easily measured. These parameters are important to consider when trying to determine the causes for variations in breeding success and are usually regarded as necessary information for interpreting changes. The following is a brief description of these other parameters.

4.3.3.1 Laying date

Food availability can lead to variation in the date of egg laying within populations between years (Birkhead and Harris 1985, Becker 1996). Environmental conditions that influence food abundance or accessibility, such as the extent of sea ice or stormy weather, may also be negatively correlated with laying date.

4.3.3.2 Clutch size

The number of eggs laid may depend on food availability in the breeding season (e.g., Monaghan et al. 1992, Pons 1992). There is also a balance between the number of eggs produced and the size and/or quality of each egg (Birkhead and Harris 1985). Species that lay a single-egg clutch cannot vary the size of their clutch.

4.3.3.3 Egg size and quality

Egg size can decline under conditions of low food availability (Pons 1992, Bolton et al. 1992). Species that lay a single- egg clutch can regulate their reproductive effort by varying egg size or the amount of resources allocated to the egg (Birkhead and Harris 1985). Considerable variation in egg size (25–30 %) occurs among and within auk populations (Birkhead and Harris 1985). This reflects variation in female mass or body condition and, thus, egg size is indirectly affected by food availability through adult body condition. But egg size depends on other confounding factors such as age of the bird (and averages therefore vary with the age structure of the population). Egg quality may respond in a non- linear fashion to variations in food supply.

4.3.3.4 Chick provisioning rates

See Section 4.4

4.3.3.5 Causes of egg and chick mortality

The separation of external and intrinsic factors causing egg mortality may give information on possible pollution problems by toxic contaminants, the percentage of infertile eggs and on egg predation. Investigation of the fate of the chicks can help in differentiating between various causes of mortality (e.g., Thyen et al. 1998).

4.3.3.6 Growth rates of chicks

Growth rates may depend on food availability during the chick rearing period (Gaston 1985, Mlody and Becker 1991, Klaassen et al. 1992). There is a close relationship between the supply of young herring and the growth rate of chicks that fledge in common terns breeding in the Wadden Sea (Greenstreet et al. 1999). Chick growth will reflect foraging conditions especially in species that cannot alter their time budgets (some Procellariformes, terns). However, in many seabirds chick growth occurs at the maximum rate possible and is insensitive to food abundance unless this is severely reduced.

4.3.3.7 Mass of fledglings

Fledging mass depends on food availability during the breeding season, varies between years and reflects the amount of energy reserves of fledgling and, thus, how long a bird can withstand starvation. Therefore, mass at fledgling should be positively correlated with the probability of recruitment to the breeding population (Becker et al. 2001, Hipfner 2000). This has been shown to be the case in several, but not all, seasons for a number of species. The rate of provisioning depends also on food availability and again varies considerably among and within populations and years (Gaston 1985) so it should be positively correlated with fledging mass. But some seabirds have flexible time and energy budgets during the breeding season and are thus able to maintain provisioning rates under moderate declines in foraging conditions (Burger and Piatt 1990).

4.3.3.8 Reproductive success

Reproductive success as the final outcome of the reproductive performance in a season may be the least sensitive parameter in reflecting prey availability or foraging conditions because it is influenced by other factors like predation, weather or flooding. However, these can often be recorded and controlled for.

4.3.4 Possibilities for integrated seabird population monitoring

The use of seabirds as monitors of the marine environment is becoming increasingly widespread. Monitoring of parameters other than population size is usually regarded as necessary information for interpreting changes. As is shown above, the relevance of the various population parameters will depend on the life history of the species concerned. For extreme long-lived species the order of parameters measured may be adult survival, subadult survival and breeding success.

The different population parameters integrate environmental effects over different time spans. Different lag times before the effects can be measured and different accuracies with which effects are likely to be detected have to be considered (Croxall et al. 1988).

Long-term integrated monitoring of seabird populations is costly and thus rare (Nisbet 1989, Wooller et al. 1992). Nevertheless, there are some good examples of integrated long term studies at “constant effort sites”: wandering albatross (Weimerskirch et al. 1987, Croxall et al. 1992, Weimerskirch 1999), short-tailed shearwater (Wooller et al. 1989, Bradley et al. 1991, 1999), black-legged kittiwake (Coulson and Thomas 1985, Porter and Coulson 1987, Thomas and Coulson 1988; Danchin et al. 1998, Cam et al. 1998); Atlantic puffin (Harris and Wanless 1991, Harris et al. 1997); great skua (Furness 1987); common tern (Becker and Wendeln 1997, Becker et al. 2001). Such studies require special sites which allow good access, a long term perspective, an committed team of researchers, the necessary financial basis and effective data management (Bradley et al. 1991). In addition the use of new field techniques, e.g., field readable rings or remote and automatic recording of subadults and adults by passive transponders (Becker and Wendeln 1997, Becker et al. 2001) may help to increase the efficiency of integrated population monitoring in seabirds.

It is clear that different species of seabirds respond differently to environmental change, depending on their particular life history strategies, and that the ideal programme of seabird monitoring would consider not only breeding numbers and breeding success, but would include attention to other aspects of seabird life history parameters, especially adult survival, subadult survival and recruitment rate, as well as parameters of reproductive performance.

4.4 Seabird diets and provisioning as monitors of fish stocks and food availability

Dietary composition of seabirds can often be sampled easily and has been used to monitor prey stocks (Montevecchi 1993). Some studies have demonstrated statistically significant correlations between commercially harvested fish stocks and their relative abundance in seabird diets. The proportion of sandeel in the diet of great skua chicks was positively correlated with the number of sandeels recruited to the Shetland population in the previous year (Hamer et al. 1991). Coincidental collapses have been reported in the proportion of squid in northern gannet diet and in the squid fishery off Canada (Montevecchi 1993). Sampling of regurgitated pellets at colonies or roost sites provides otoliths from these fish that can be identified to species, measured to give fish size and sectioned to count annual layers to determine fish age (Barrett et al. 1990). This approach has not addressed the problem that such measures represent relative availability of prey only. Then, it is necessary to compare harvest prey by seabirds and fisheries. The relative abundance of fish taken by birds and fisheries could correspond closely but the spatial and temporal scales over which acoustic surveys conducted by fisheries scientists and seabird foraging may be incorrectly matched. The proportion of a particular species in seabird diet may closely reflect absolute abundances at low levels of biomass but may not be sensitive when prey availability is high (Becker et al. 1987). The development of robust indices requires the inclusion of other seabird parameters that, considered together, are sensitive to change in prey over a large range of absolute abundances (Cairns 1987).

Variation in parental food loads and in chick provisioning rates could also be obtained in species that carry food in their bills like terns or Atlantic puffins. Among multi-prey loaders, inverse relationships between number of items carried per trip and total masses of food loads suggest that the number of items carried may yield a crude index of prey conditions, i.e., fewer, larger items when food supplies are good (Barrett et al. 1987). The chick-provisioning rates can be ranked according to good, intermediate and poor prey conditions.

4.5 Recommendations for further monitoring marine pollution using seabirds as accumulative indicators

4.5.1 Background

Pollution may affect seabirds in many ways as seabirds are marine top predators that biomagnify contaminants to high concentrations. Contaminants have the potential to affect life history parameters, especially during the sensitive phase of reproduction, and parameters such as egg shell thickness, embryonic survival, hatching success, chick growth or reproductive success have been found to be impaired in several studies. The high biomagnification rates qualify marine

birds also as monitors of pollutants (ICES 1999). The potential influence of contaminants on seabird life history parameters means that any integrated seabird monitoring programme should take full account of them.

In some parts of the North Sea monitoring pollutants by seabirds as accumulative indicators occurs already (see below) but should be expanded to other areas of the North East Atlantic, using further species as monitors.

4.5.2 Oil

Ongoing programmes of monitoring of the proportions of dead and oiled seabirds found on shorelines (‘Beached Bird Surveys’ - BBS) should be encouraged as a cost effective means (most are carried out by amateurs at no cost and are organised by NGOs) of determining long-term trends and geographical patterns of oil pollution at sea (Camphuysen and Heubeck 2001). Such monitoring is of greater interest to seabird conservation than to fisheries. BBS is carried out along all the North Sea coasts, and implemented in the TMAP (Trilateral Monitoring and Assessment Programme of the Wadden Sea).

4.5.3 Plastic particles

Numbers of plastic pellets in the oceans appear to be continuing to increase and there is a need to monitor the amounts of plastic ingested by seabirds, especially petrels. Some effects of ingested plastics on seabirds have been noted. Seabirds may provide a useful indicator of this form of pollution.

4.5.4 Organochlorines

Sampling of seabird eggs as a means of monitoring local contamination with organochlorines should be included in integrated marine pollution monitoring programmes, with the selection of appropriate locally common and internationally widespread monitoring species (ICES 1999). In the Wadden Sea, within TMAP, the monitoring of organochlorines as well as of mercury in eggs has occurred since 1996 (Becker et al. 1998, Thyen and Becker 2000). In the Swedish Marine Monitoring Programme common guillemot eggs have been used as indicators of Baltic Sea pollution since the 1960s (Bignert et al. 1998). Seabird eggs are already included in the JAMP guidelines for monitoring organochlorine contaminants in biota (OSPAR 1997).

4.5.5 Mercury

Methods to monitor mercury contamination in marine food chains by sampling chick down or feathers from chicks or adults, or from blood samples or egg samples, have been developed and are standardised. Monitoring of mercury levels using these methods should be carried out in areas where there is concern about possible mercury contamination of marine food chains. Eggs sampled from colonies located close to rivers contaminated with mercury can be used as a means of monitoring trends in river mercury loadings reaching the sea. Such monitoring can also provide useful evidence of the success of programmes to reduce mercury. Seabird eggs are included in the JAMP guidelines for monitoring mercury in biota (OSPAR 1997).

4.5.6 Organotin and other metals

There is a need for research into organotin levels in seabirds to determine whether these may have toxic effects on seabirds, and whether seabirds may be used as a means of monitoring organotin pollution on large scales.

There is also a need for research into the possible use of eggshells, egg contents or feathers for monitoring cadmium, lead and other elemental concentrations. At present, monitoring of levels of these pollutants involves killing of birds to sample liver, kidney or bones. In particular, if methods can be developed to measure elemental concentrations within feather keratins separately from contaminants on feather surfaces, this would permit retrospective monitoring, using museum specimens, of long term trends in elemental contamination of marine food chains as has been done successfully for mercury.

4.6 Further aspects of designing monitoring programmes with seabirds

An important issue is also the spatial scale at which the processes of interest are occurring and thus the spatial scale at which monitoring needs to be carried out. Seabirds can breed in large discrete colonies. Good sample sizes are therefore possible for monitoring local parameters on series of discrete sub-units of the population, but it has lead in the past to

the concentration of efforts on a very limited number of “key” sites, usually where long-term studies have been taking place. When considering which parameters could be good to monitor, special effort should thus be put in

1) considering the representativeness of the monitored sites, 2) integrating the monitoring of the parameters on series of sites at different scales (e.g., choice of colonies at a regional scale and choice of study plots within a colony), and 3) combining various indicative parameters into an integrated monitoring project.

However, for those species breeding on cliffs the choice of sites is constrained by ease of access.

The Working Group noted that for logistical reasons there is an understandable concentration of monitoring at “key” sites, but also noted that additional and powerful analyses become possible if the key sites are supplemented by a wider net of sites (Anker-Nilssen et al. 1996). This may be especially important as this allows questions about the spatial dependence and scale of change in the parameters monitored to be addressed. For instance, variability in some seabird population parameters may suggest independence in variability among fish stocks of different areas (Furness et al. 1996). Monitoring parameters at different locations in an integrated fashion is also crucial because of the potential importance of movements of individuals between sites and the effect that this can have on demography. This has classically been neglected due to the high natal philopatry and breeding philopatry of individuals of most species and the difficulty of quantifying the rates of movement among locations (Boulinier and Lemel 1996). There is evidence that dispersal of individuals may be dependent on local conditions and can affect strongly local numbers of breeders (e.g., dispersal of breeding individuals among kittiwake colonies situated few kilometres apart (Danchin et al. 1998). Further, statistical modelling tools are now available to estimate rate of dispersal between locations while accounting for different probability of individuals being sighted or dying in the different locations (Spendelow et al. 1995). Finally, the availability of time series of comparable data from several locations can allow stronger inference to be made. This is because an analysis carried out on the time series analyses from only one site may suffer the weakness of the potential existence of several alternative factors driving the observed pattern. Monitoring interactions of trends in a parameter among several sites in relation to external parameters allows more powerful diagnosis of factors responsible for changes (e.g., Anker-Nilssen et al. 1996, Thyen et al. 1998). Study colonies should, where possible, be selected on the basis of the likelihood of changes in those variables that can affect seabirds.

4.7 References

Aebischer, N. J., Coulson, J. C. and Colebrook, J. M. 1990. Parallel long-term trends across four marine trophic levels and weather. Nature 347: 753–755.

Anderson, D. W., Gressand F. and Mais K. F. 1982. Brown pelicans: influence of food supply on reproduction. Oikos 39: 23–31.

Anker-Nilssen, T., Erikstad, K. E., and Lorentson, S. H. 1996. Aims and effort in seabird monitoring: an assessment based on Norwegian data. Wildlife Biology 2: 17–26.

Barrett, R. T., Anker-Nilssen, T., Rikardsen, F., Valde, K., Rov, N. and Vader, W. 1987. The food growth and fledging success of Norwegian puffin chicks Fratercula arctica in 1980–1983. Ornis Scandinavica 18: 73–83.

Barrett, R. T., Rov, N., Loen, J. and Montevecchi, W. A. 1990. Diets of shags Phalacrocorax aristotelis and cormorants P. carbo in Norway and implications for gadoid stock recruitment. Marine Ecology Progress Series 66: 205–218.

Becker, P. H. 1996. Flußseeschwalben (Sterna hirundo) in Wilhelmshaven. - Oldenburger Jahrbuch 96: 263–296.

Becker, P. H. 1998. Langzeittrends des Bruterfolgs der Flußseeschwalbe und seiner Einflußgrößen im Wattenmeer. Vogelwelt 119: 223–234.

Becker, P. H., Frank, D. and Walter, U. 1987. Geographische und jährliche Variation der Ernährung der Flußseeschwalbe (Sterna hirundo) and der Nordseeküste. Journal für Ornithologie 128: 457–475.

Becker, P. H., Thyen, S. Mickstein, S., Sommer, U. and Schmieder, K.R. 1998. Monitoring pollutants in coastal bird eggs in the Wadden Sea. Final Report of the Pilot Study 1996–1997.Wadden Sea Ecosystem 8. Common Wadden Sea Secretariat Wilhelmshaven: 59–101.

Becker, P. H. and Wendeln, H. 1997. A new application for transponders in population ecology of the common tern. Condor 99: 534–538.

Becker, P. H., Wendeln, H. and González-Solís, J. 2001. Population dynamics, recruitment, individual quality and reproductive strategies in common terns marked with transponders. Ardea, in press.

Bignert, A., Olsson, M., Persson, W., Jensen, S., Zakrisson, S., Litzen, K., Erksson, U., Haggberg, L. and Alsberg, T. 1998. Temporal trends of organochlorines in Northern Europe, 1967–1995. Relation to global fractionation, leakage from sediments and international measures. Environmental Pollution 99, 177–198.

Birkhead,T. R. and Harris, M. P. 1985. Ecological adaptations for breeding in the Atlantic Alcidae. pp.205–231. In D.N. Nettleship and T.R. Birkhead (eds.). Atlantic Alcidae. Academic Press, London.

Boersma, P. D. 1978. Breeding patterns of Galapagos penguins as an indicator of oceanographic conditions. Science 200: 1481–1483.

Bolton, M., Houston, D. and Monaghan, P. 1992. Nutritional constraints on egg formation in the lesser black-backed gull: an experimental study. Journal of Animal Ecology 61: 521–532.

Boulinier, T. and Lemel, J.-Y. 1996. Spatial and temporal variations of factors affecting breeding habitat quality in colonial birds: some consequences for dispersal and habitat selection. Acta Oecologica 17: 531-552.

Bradley, J. S., Gunn, B.M., Skira, I. J., Meathrel, C. E. and Wooller, R. D. 1999. Age-dependent prospecting and recuitment to a breeding colony of short-tailed shearwaters Puffinus tenuirostris. Ibis 141: 277–285.

Bradley, J. S., Skira, I. J. and Wooller, R. D. 1991. A long-term study of short-tailed shearwaters Puffinus tenuirostris on Fisher Island, Australia. Ibis 133, Supplement 1: 55–61.

Burger, A. E. and Piatt, J.F. 1990. Flexible time-budgets in breeding common murres: buffers against variable prey abundance. Studies in Avian Biology 14: 71–83.

Cairns, D. K. 1987. Seabirds as indicators of marine food supplies. Biological Oceanography 5: 261–271.

Cam, E., Hines, J. E., Monnat, J.-Y., Nichols, J. D. and Danchin, E. 1998. Are adult nonbreeders prudent parents? The kittiwake model. Ecology 79, 2917–2930.

Camphuysen, C. J. and Heubeck, M. 2001. Marine oil pollution and beached bird surveys: the development of a sensitive monitoring instrument. Environmental Pollution 112: 443–461.

Coulson, J. C. and Thomas, C. 1985. Differences in the breeding performance of individual kittiwake gulls, Rissa tridactyla. pp. 489–503. In: Sibly, R.M. and Smith, R.H. (eds.): Behavioural Ecology, Blackwell, Oxford.

Croxall, J. P., McCann, T. S., Prince, P. A. and Rothery, P. 1988. Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976–1987: implications for Southern Ocean monitoring studies. Pp 261–285 in Sahrhage, D. (Ed.) Antarctic and Ocean Resources Variability. Springer Verlag, Berlin.

Croxall, J. P. and Rothery, P. 1991. Population regulation of seabirds: implication of their demography for conservation. pp. 272–296. In C. M. Perrins, J.D. Lebreton and Hirons, G. J. M. (eds) Bird population studies: relevance to conservation and management. Oxford University Press, Oxford.

Croxall, J. P., Rothery, P. and Crisp, A. 1992. The effect of maternal age and experience on egg-size and hatching success in wandering albatrosses Diomedea exulans. Ibis 134: 219–228.

Danchin, E., Boulinier, T. and Massot, M. 1998. Habitat selection based on conspecific reproductive success: implications for the evolution of coloniality. Ecology 79, 2415–2428.

Furness, R. W. 1993. Birds as monitors of pollutants. In: Furness, R. W. and Greenwood, J. J. D. Birds as monitors of environmental change. pp. 86–143. Chapman and Hall, London.

Furness, R. W. 1987. The skuas. Poyser, Calton

Furness, R. W. and Greenwood, J. J. D. 1993. Birds as monitors of environmental change. Chapman and Hall, London

Furness, R. W. and Nettleship, D. N. 1990. Seabirds as monitors of changing marine environment. Acta XX Congressus Internationalis Ornithologici: 2239–2240.

Furness, R. W., Greenstreet, S. P. R. and Walsh, P. M. 1996. Spatial and temporal variability in the breeding success of seabirds around the British Isles: evidence for distinct sandeel stocks. ICES Cooperative Research Report 216: 63–65.

Gaston, A. J. 1985. Development of the young in the Atlantic Alcidae. pp.319–352. In D.N. Nettleship and Birkhead, T.R. (eds.) Atlantic Alcidae. Academic Press, London.

Greenstreet, S .P. R., Becker, P. H., Barrett, R., Fossum, P. and Leopold, M. F. 1999. Consumption of pre-recruit fish by seabirds and the possible use of this as an indicator of fish stock recruitment. In Furness, R. W. and Tasker, M. L. (eds.) Diets of seabirds and consequences of changes in food supply. ICES Cooperative Research Report 232: 6–17.

Hamer, K. C., Furness, R. W. and Caldow, R. W. G. 1991. The effects of changes in food availability on the breeding ecology of great skuas Catharacta skua in Shetland. Journal of Zoology, London 223: 175–188.

Harris, M. P. and Wanless, S. 1991. Population studies and conservation of puffins Fratercula arctica. pp. 230–248. In Perrins, C. M., Lebreton, J.D. and Hirons, G.J.M. (eds.) Bird population studies: relevance to conservation and management. Oxford University Press, Oxford.

Harris, M. P., Halley, D. J. and Wanless, S. 1992. The post-fledging survival of young guillemots Uria aalge in relation to hatching date and growth. Ibis 134: 335–339.

Harris, M. P., Freeman, S. N., Wanless, S., Morgan, B. J. T. and Wernham, C.V. 1997. Factors influencing the survival of puffins Fratercula arctica at a North Sea colony over a 20-year period. Journal of Avian Biology 28: 287–295.

Hipfner, M. 2000. Fitness consequences of replacement egg-laying for arctic-nesting thick-billed murres. Proceedings 7th Seabird Group Conference Wilhelmshaven, 25.

Hunt, G. L., Eppley, Z. A. and Schneider, D.C. 1986. Reproductive performance of sea-birds: the importance of population and colony size. Auk 103: 306–317.

Hunt, G. L., Jr. and Schneider, D. C. 1987. Scale-dependant processes in the physical and biological environment of marine birds. In: Croxall, J. P. (ed.) Seabirds, feeding ecology and role in marine ecosystems, pp. 7–41. Cambridge University Press, Cambridge.

ICES. 1999. Report of the Working Group on Seabird Ecology. ICES CM 1999/C:5.

ICES. 2000. Report of the Working Group on Seabird Ecology. ICES CM 2000/C:04.

Klaassen, M., Zwaan, B., Heslenfeld, P., Lucas, P. and Luijckx, B. 1992. Growth rate associated changes in the energy requirements of tern chicks. Ardea 80: 19–28.

Lebreton, J. D., Burnham, K. P., Clobert, J. and Anderson, D. R. 1992. Modelling survival and testing hypotheses using marked animals: a unified approach with case studies. Ecological Monographs 62: 67–118.

McNamara, J. M. and Houston, A. I. 1996. State-dependent life histories. Nature 380: 215–221

Mlody, B. and Becker, P. H. 1991. Körpermasse-Entwicklung und Mortalität von Küken der Flußseeschwalbe (Sterna hirundo L.) unter ungünstigen Umweltbedingungen. Vogelwarte 36: 110–131.

Monaghan, P., Uttley, J. D. and Burns, M. D. 1992. Effects of changes in food availability on reproductive effort in arctic terns. Ardea 80: 71–81.

Montevecchi, W. A. 1993. Birds as indicators of change in marine prey stocks. Pp. 217–265. in Furness, R. W. and Greenwood, J. J. D. (eds.) Birds as monitors of environmental change. Chapman and Hall, London.

Montevecchi, W. A., and Berruti A. 1990. Avian indication of pelagic fishery conditions in the southeast and north-west Atlantic. Acta XX Congressus Ornithologici: 2246–2256.

Nisbet, I. C. T. 1989. Long-term ecological studies of seabirds. Colonial Waterbirds 12: 143–147.

Oro, D. and Pradel, R. 2000. Determinants of local recruitment in a growing colony of Audouin's Gull. Journal of Animal Ecology 69: 119–132.

OSPAR. 1997. JAMP guidelines for monitoring contaminants in biota. 9/6/97, Oslo.

Pons, J.-M. 1992. Effects of changes in the availability of human refuse on breeding parameters in a herring gull Larus argentatus population in Brittany, France. Ardea, 80: 143–150.

Porter, J. M. and Coulson, J. C. 1987. Long-term changes in recruitment to the breeding group, and the quality of recruits at a kittiwake Rissa tridactyla colony. Journal of Animal Ecology 56: 675–690.

Roff, D. A. 1992. The evolution of life histories: theory and analysis. Chapman and Hall, New York.

Schreiber, R. W. and Schreiber, E. A. 1984. Central Pacific seabirds and the El Nino southern oscillation: 1982 to 1983 perspectives. Science 225: 713–716.

Spendelow, J. A., Nichols, J. D., Nisbet, I. C., Hays, H., Cormons, G. D., Burger, J., Safina, C., Hines, J. E. and Gochfeld, M. 1995. Estimating adults survival and movement rates of adults within a metapopulation of roseate terns. Ecology 76: 2415–2428.

Stearns, S. C. 1992. The evolution of life histories. Oxford University Press, Oxford.

Thomas, C. S. and Coulson, J. C. 1988. Reproductive success of kittiwake gulls, Rissa tridactyla. Pp 251–262 in T.H. Clutton-Brock, (ed) Reproductive success. University of Chicago Press, Chicago.

Thyen, S. and Becker, P.H. 2000. Aktuelle Ergebnisse des Schadstoffmonitorings mit Küstenvögeln im Wattenmeer. Vogelwelt 121: 281–291.

Thyen, S., Becker, P. H., Exo, K.-M., Hälterlein, B., Hötker, H. and Südbeck, P. 1998. Monitoring breeding success of coastal birds. Final report of the pilot study 1996–1997. Wadden Sea Ecosystem 8. Common Wadden Sea Secretariat Wilhelmshaven: 8–55.

Weimerskirch, H. 1999. The role of body condition on breeding and foraging decisions in albatrosses and petrels. pp.1178–1189 in Adams, N. J. and Slotow, R. H. (eds.) Proceedings 22nd Int. Ornithological Congress, Durban. Johannesburg: BirdLife South Africa.

Weimerskirch, H., Clobert, J. and Jouventin, P. 1987. Survival in five southern albatrosses and its relationship with their life history. Journal of Animal Ecology 56: 1043–1055.

Wooller, R. D., Bradley, J. S. and Croxall, J. P. 1992. Long-term population studies of seabirds. Trends in Ecology and Evolution 7, 111–114.

Wooller, R. D., Bradley, J. S., Skira, I. J. and Serventy, D. L. 1989. Short-tailed shearwater. Pp. in Newton, I. (ed.) Lifetime reproduction in birds. Academic Press, London.

5 REVIEW OF THE INTERACTIONS BETWEEN AQUACULTURE AND BIRDS IN THE ICES AREA

5.1 Introduction

The aim of this review is to provide to ICES, and specifically to the ICES Working Group on Environmental Interactions of Mariculture, a brief review from the perspective of seabird ecologists of the interactions between aquaculture and birds. There has been a huge growth in aquaculture in the last few decades, with consequent concerns for a variety of environmental impacts (Naylor et al. 2000). In temperate and higher latitudes, this has particularly involved marine cage culture of high value finfish, such as Atlantic salmon, and various forms of marine culture of shellfish.

Aquaculture can provide new feeding opportunities for some birds, and so can create a local increase in bird numbers. Increases in bird numbers at fish farms may lead to problems for fish farmers. Birds may eat or damage stock, may represent a nuisance or a vector of disease. These problems may cause significant costs to fish farmers both in direct financial terms, and in terms of time spent in trying to reduce bird problems. The impacts of birds on fish farming can lead to farmers taking action against perceived bird problems, while farming itself may have some negative impacts on birds. Direct negative effects of aquaculture on seabirds (defined here as marine birds and shorebirds) have been thought to arise mainly from loss of habitat, harvest of young marine animals for culture that may represent natural food of some seabirds, disturbance of birds by fish farm workers, and killing of birds (either deliberately or accidentally). It should be noted that enhancing food supply to wildlife is not necessarily a positive effect, since increases in some animal populations can have negative impacts on others, and can lead to populations becoming dependent on artificial feeding opportunities. Aquaculture may also have indirect effects on seabird populations, since most fish farms in ICES areas are dependent on the use of aquafeeds derived largely from fish meal and fish oils (Thomson 1990, Naylor et al. 2000). This raises the indirect effects of industrial fishing on seabirds as an issue related to the practice of mariculture.

In this review the topics are considered in the following sequence: Enhancing food supplies to wildlife: common eider; shorebirds; gulls; seals, cormorants, herons and other birds; attraction of birds to aquaculture and consequent impacts on fish farming profitability; disturbance of birds by aquacultural activities; persecution of birds by fish farmers; impacts on birds of the harvest of mussel spat; impacts of industrial fishing on seabirds. Certain aspects that may be relevant have not been reviewed here due to lack of appropriate expertise, and lack of access to literature on the subject area; these include wild birds as vectors of diseases affecting cultured fish and shellfish (Erwin 1995, and see for example Moravec et al. 1997 who report parasite infections in cultivated fish where birds host the adult parasite).

5.2 Enhancing food supplies to wildlife

There are several cases where aquaculture provides food for wild animals, to an extent that certainly influences the pattern of distribution of the animals and may in some cases increase their population size. Some of the better- documented examples are outlined below.

5.2.1 Common eider

Common eiders are widely distributed sea ducks that inhabit coasts around the globe in sub-polar and boreal regions. They specialise in feeding on mussels, which they locate by diving in shallow water, pull off the substrate and swallow whole, then grind these up in their muscular gizzard. Farmed mussels grown on suspended rope cultures are particularly attractive to common eiders because these tend to be thin shelled and have a high energy content compared with wild mussels growing intertidally. They are also grown at high densities and at shallow depths, so that energy costs of feeding are minimised for common eiders allowed to feed undisturbed at mussel farms. Common eiders, and to a smaller extent also some other sea ducks such as long-tailed ducks and scoters, soon develop the habit of flocking at unprotected mussel farms where they can rapidly deplete the standing stock of cultivated mussels (Milne and Galbraith 1986, Ross and Furness 2000). Although experienced farmers tend to take steps to deter ducks from stealing cultivated mussels, many farms do not protect their stock very effectively, and common eider numbers feeding on farms can represent a high proportion of the local population. This is particularly the case in spring, when female common eiders need to feed intensively in order to build up reserves for egg production and for their fast throughout incubation. Somewhat unexpectedly, winter surveys of common eiders feeding on natural habitat, at mussel farms and at salmon cages in the west of Scotland (Figure 5.1) found that common eiders fed in very large numbers at many salmon farms as well as at mussel farms. In general, salmon farmers do not scare common eiders away and the ducks evidently learn this. They often roost in close proximity to salmon farms, where human disturbance may be reduced compared to other stretches of coastline, due to salmon farms preventing human access to reduce risks of disease transmission. It is not clear whether common eiders feeding around salmon cages are simply stripping off mussels that foul the cages, nets and ropes, or whether common eiders also scavenge lost fish pellet food. Certainly, captive common eiders will happily feed

on salmon feed pellets. Whichever is the case, there is no doubt that both mussel farms and salmon farms attract common eiders, and in the west of Scotland they have a strong influence on their local distribution from autumn to spring. Despite this strong, and relatively new, feeding association, there is no convincing evidence from detailed and accurate census data that the opportunities to feed at salmon and mussel farms has influenced population sizes of common eiders in Scotland.

Feeding sites used by common eiders in various areas of west Scotland

120

100 Eiders feeding at salmon 80 farms Eiders feeding at mussel 60 farms 40 Eiders in natural feeding 20 habitat

Percent of eiders in area 0 123456 Area

Figure 5.1. Percentages of common eiders in six areas in the west of Scotland that were in feeding flocks at salmon farms, at mussel farms and at natural habitat in surveys in autumn-winter 1998 and 1999. Large differences between areas reflect differences in numbers of aquaculture establishments in different areas as well as variations in common eider habits (based on data in Ross and Furness 2000).

5.2.2 Shorebirds

Many species of shorebirds spend the winter feeding on intertidal benthic invertebrates on estuaries and sheltered coasts. Where aquaculture is established on intertidal areas, high densities of cultivated animals may present unusually good feeding opportunities for some shorebirds. In particular, Eurasian oystercatchers may benefit from being able to feed on mussels that have been artificially set on intertidal areas. Such opportunities are probably rather limited, as costs of disturbance will often outweigh the benefits from enhanced food stocks.

5.2.3 Gulls

Many species of gulls are highly opportunistic feeders, and exploit a wide range of habitats as well as taking many kinds of food. Where aquaculture permits access to gulls, they will readily scavenge on remains of fish and invertebrates, steal aquafeed pellets from feeders or by tearing open carelessly stored bags of feed, and take the growing product from accessible areas on farms. This is especially true of herring gulls. Gulls do not need to spend much time feeding each day, but can often obtain most of their daily energy needs in a few minutes of intense feeding at a place where food is abundant. It is very common to see flocks of several hundred gulls hanging around aquaculture facilities waiting for occasional opportunities to feed at the farmers’ expense. There is no doubt that the local distribution of gulls can be affected by the availability of such feeding opportunities, but populations of gulls use aquaculture as only a small part of their overall energy intake, and it is unlikely that this has much effect on gull population sizes. It is possible that the local aggregations of large scavenging gulls at aquaculture sites may drive away smaller birds that can be the target of robbery or predation by gulls.

5.2.4 Seals, cormorants, herons and other birds

Unprotected fish farms can attract seals, and a variety of piscivorous birds, especially some species of cormorants (Nettleship and Duffy 1995) and herons (Kushlan 1997). The fact that these animals gather at fish farms implies that they find that these sites provide an attractive feeding opportunity (Price and Nickum 1995). Often the animals attracted to fish farms are predominantly young ones, suggesting that adult animals perceive the hazards of feeding at fish farms

to outweigh the benefits of access to easy pickings. Young animals are generally less efficient at foraging and are often displaced from the best feeding sites by older, dominant, animals. The inferior abilities of young animals may make fish farms relatively more attractive to them because they present a chance for rapid food intake, albeit at a high risk. Young animals at increased risk of starvation may find that feeding at fish farms increases their chances of overwinter survival providing they are not subject to high risks of being shot by farmers.

Fleury and Sherry (1995) reported that winter populations of wading birds (mostly herons) increased dramatically in Louisiana between 1966 and 1989, and that increased acreage devoted to crayfish Procambarus aquaculture appeared to be the main factor explaining this increase. Wading bird numbers correlated over years with crayfish pond acreage, and birds used this feeding habitat extensively, especially during pond drawdowns that took place during the birds’ breeding season and may have increased reproductive output. In addition, the greatest population increases were in the bird species making most use of crayfish as food.

5.3 Attraction of birds to aquaculture and consequent impacts on fish farming profitability

Where aquaculture attracts large numbers of birds, the activities of the birds may represent a serious impact on the profitability of farming, as a result of birds taking product or interfering with the functioning of the farm. The main perceived impacts on farming are depredations of fish by cormorants and herons, and depredations of mussels by sea ducks (especially common eiders). Few studies in the ICES area have quantified costs, so we provide examples from studies elsewhere in the world that are relevant and instructive. Many of these refer to freshwater aquaculture sites, where quantifying damage or losses is easier.

Glahn et al. (1999a) conducted on-site interviews of fish farmers in the north-eastern United States, and made brief bird counts at these sites during summer visits (not necessarily the season when most birds feed at fish farms). They reported that 80% of fish farmers reported bird predation to be a problem at their site, great blue herons being the main concern, and trout farmers the most affected group. Nearly a quarter of trout farms were thought to be losing stock worth more than US$10,000 per year to bird predation. Great blue herons were seen at 90% of aquaculture sites they visited. Further investigation involved shooting herons at these sites to investigate stomach contents. Herons showed crepuscular feeding habits, ingesting about three trout per day per bird, mainly taking fish in the 12–38 cm length range (Glahn et al. 1999b). Trout losses varied between sites, being negligible at some sites not visited by herons, but up to 40% of trout stock was taken at other sites where herons were frequent visitors.

Avery et al. (1999) studied fish loss due to bird predation (mainly by herons and egrets) at aquaculture ponds in central Florida. Losses from ponds from which birds were excluded by netting averaged 11% while losses from ponds without netting averaged 38% of fish stock. These translated to economic losses of US$589 per netted pond and US$1360 per un-netted pond, making anti-predator netting highly cost effective even though not fully successful in preventing predation.

Costa-Pierce (1998) reported that bird predation was responsible for loss of about 50% of tilapia stocked in combined wastewater treatment-fish culture ponds in Los Angeles County. Pitt and Conover (1996) reported that herons (great blue herons and black-crowned night herons), ospreys and California gulls were the main predators of fish at Intermountain West fish hatcheries. Birds were estimated by scientific study to remove 7% and 0.5% of annual production from two hatcheries, whereas managers estimated losses to birds at 15% at each of these two hatcheries. Managers at private hatcheries estimated losses to birds at 13% of production, whereas managers of state-owned hatcheries estimated losses to birds at only 5%.

In the Mississippi Delta of the United States, catfish farmers estimated loss to cormorants of fish worth US$3.3 million per year. A bioenergetics model combined with data on cormorant numbers and diet, suggested that double-crested cormorants may have eaten up to 20 million catfish per winter in 1989–90 and 1990–91 in the Delta region of Mississippi, equating to 4% of standing crop at an estimated replacement cost of US$2 million per year (Glahn and Brugger 1995), which is not too far from the farmers’ estimate of the cost of bird predation given that farmers are likely to provide estimates that maximise the scale of the problem.

Predation by grey herons and great cormorants was studied by Genard et al. (1993) in a dyked area intended for extensive brackish water aquaculture on the French Atlantic coast. A pond was divided in two parts, one of 0.9 ha was protected with nets and wires, while the other of 0.3 ha was left without protection. Fish (Mugilidae) were stocked in November, during the wintering period of the birds. Three weeks later, remaining fish in both parts of the ponds were counted. The number, presence and predation behaviour of birds was observed during the experiment. A spectacular but temporary gathering of birds occurred during the first days following fish stocking. Cormorants used deeper and herons shallower areas of the pond. Intensity of predation attempts was higher among cormorants. Features of predation exerted by these birds were the rapid exhaustion of the fish population, the higher predation level by cormorants than by

herons, although the latter obtained a very high success ratio (number of catches/number of attacks) (Genard et al. 1993). Similar studies of fish ponds that could be drained to count numbers of surviving fish after a period of exposure to bird predation were carried out recently in England to try to quantify the impact of predation by herons and especially cormorants. That study had difficulty with assessment of nocturnal feeding by birds, but also suggested that piscivorous birds can remove stocked fish rather rapidly from small ponds (McKay et al. 1999).

Common eiders, and to a lesser extent other ducks such as common goldeneye and long-tailed ducks, can rapidly deplete mussels from suspended cultures on rafts or long-line mussel farms. Many mussel farms in Scotland and in eastern Canada have been put out of business by duck predation drastically reducing cultivated stock and harvest. Most mussel farmers in Scotland regard common eiders as the main predation problem on mussel farms, and spend considerable amounts of time, and cash, in trying to combat this problem (Ross and Furness 2000).

Not all studies of bird ‘problems’ at fish farms support the view of managers that birds cause significant economic losses. For example, Ulenaers and van Vessem (1994) showed that great crested grebes at a freshwater fish farm in the Netherlands only marginally influenced fish populations in the ponds despite farmers’ claims that they took large amounts of fish.

5.4 Disturbance of birds by aquacultural activities

Aquaculture can cause disturbance to wildlife by major modification of habitat, such as removal of habitat required for nesting or feeding sites. It can also cause local disturbance through minor alterations to habitat. For example, oyster culture on intertidal areas involves addition of racks, stakes, culture bags, marker poles and other equipment onto open tidal flats. Some birds are attracted onto such structures. For example, gulls (and some kinds of shorebirds) may use elevated structures as roosts. However, most species of shorebirds tend to avoid oyster culture plots, preferring to feed on open areas of tidal flats. Since shorebird numbers tend to be set by the amount of food in their wintering estuaries, loss of open estuarine foraging habitat to aquaculture is likely to have a negative impact on shorebird populations. This has not been studied in detail as yet. Aquaculture probably has much less impact on shorebirds than does loss of estuarine habitat through land claim or alteration of invertebrate populations due to nutrient pollution, but loss of feeding area to shorebirds through aquaculture will add to these other forms of habitat loss that are concerns in the conservation of shorebird populations.

Human activity at aquaculture facilities can also affect wildlife. Where fish farms are sited in remote areas, as with many salmon farms or mussel farms in Scotland, wildlife may be affected by human disturbance resulting from routine farming activities in a way that animals would not be in places where they have become used to regular human activity. For example, black-throated divers nesting on remote lakes may be severely disturbed by helicopter flights transporting live fish into or from a farm, leaving their eggs exposed to predation by gulls or crows. Sea ducks may abandon otherwise profitable foraging areas if the level of disturbance by human activity increases their activity costs and reduces time available for foraging so that they are unable to balance their budget. Smaller birds, nervous of the potential threats presented to them by large gulls, may abandon an area in which large aggregations of gulls have come to gather as a result of feeding opportunities provided by aquaculture.

Disturbance of birds by aquaculture is not necessarily restricted to effects on seabirds. Mooney (1998) reported without detail that populations of some coastal tropical raptors in Australia had been reduced as a result of increased disturbance in the coastal zone associated with aquacultural development as well as other forms of habitat loss and coastal development.

While loss of natural habitat to aquaculture can be a problem, so can conversion of aquaculture sites to other uses. Nelson (1993) reported that many areas of the Mai Po marshes in Hong Kong are used for pond culture of shrimps and fish, and that these provide important habitat for a varied bird and other life, including many migratory bird species. Conversion of many of these aquaculture ponds to rice fields represented a serious threat to these bird populations.

5.5 Persecution of birds by fish farmers

Many forms of aquaculture attract certain birds and marine mammals to feed on the high concentrations of food being cultivated, as described in the previous section. If no action is taken, birds and mammals can have devastating effects on the viability of farms. Farmers generally adopt one or more of three strategies. They may invest in costly structures to exclude wildlife from farms (Brugger 1995, Ross and Furness 2000) – though careful design at the initial farm construction phase might make such ‘bolt-on’ solutions less necessary. They may reduce local numbers of the problem animals by shooting or by other means (Belant et al. 2000). They may employ nonlethal deterrents that scare damaging animals away from the area (Mott and Boyd 1995, King 1996). However, many nonlethal methods have proved to be unsuccessful (Mott and Boyd 1995, Russell et al. 1996, Dorr et al. 1998, McKay et al. 1999, Ross and Furness 2000).

Nevertheless, killing of wild predators of farmed fish is generally poor management practice. There is little scientific evidence that killing predators is effective in controlling predation. There is even less evidence that it produces an economic gain for aquaculture. By killing wildlife, it may be argued that the aquaculture industry paints an unflattering picture of itself as insensitive to the environment.

Some experts argue that there is little evidence that removal of bird or mammal predators has any long-term effect on predator abundance or fish loss at farms, because removed predators are quickly replaced by others attracted to such concentrations of food (McKay et al. 1999). Advocates of lethal control of predators argue that killing a few predators scares others and increases the effectiveness of nonlethal deterrent methods (McKay et al. 1999).

The main wildlife predation problems faced by aquaculture are fish-eating aquatic mammals and birds, especially seals, cormorants and herons (Accord 1995, Trapp et al. 1995, Russell et al. 1996, McKay et al. 1999). A survey of fish farmers in north-central states of USA found a strong consensus that farmers should be allowed to kill birds on their property without permits, and an unwillingness to invest money in preventative measures. The United States Fish and Wildlife Service reported killing under permit of about 10,000 birds per year in the early 1990s, mostly double-crested cormorants, herons and egrets. These birds were killed to reduce impacts of fish-eating birds in fish farms. Mississippi Delta catfish farmers estimated loss to cormorants of fish worth US$3.3 million per year, despite shooting birds and spending US$2.1 million per year on deterring birds. However, although the last example indicates large financial costs, these represent only a few percent of the industry’s production value.

Predator control occurs in association with aquaculture in most parts of the world. Two studies of predator control at Scottish salmon and trout farms in the late 1980s estimated that around 800 grey herons, 1600 great cormorants and 1400 European shags were being killed each year in that rapidly developing industry (Carss 1994). The majority of these birds were killed illegally, only a small proportion being killed under licence from the Scottish Office. What effect does predator control have on bird populations, and can these impacts be justified by the economic gains that result? Data to answer these questions do not exist for most parts of the world. Even in countries where wildlife conservation is given a high priority and populations are carefully monitored, the facts are far from clear. Surprisingly, despite issuing licenses to permit farmers to kill birds, the USFWS has not made any definitive evaluation of the effect of shooting on population trends of cormorants, herons and egrets in the USA. Recent analyses of legal killing suggest that the numbers killed under permit are probably too small to noticeably affect bird population size, though the scale and impact of killing without permit is not evaluated. Blackwell et al. (2000) reported that the USFWS issued 26 permits to 9 aquaculture facilities in New York, New Jersey and Pennsylvania from 1985–1997, resulting in a mean of 83 birds killed under permit per year per facility. Most birds killed were herring gulls or great blue herons, and the authors considered these numbers to be negligible in relation to the bird population sizes. Belant et al. (2000) reviewed permit records for predator killing in 9 states in southeast United States from 1987–1995. Over 108,000 birds were authorised to be killed and over 64,000 were reported to have been killed. Half were double-crested cormorants, 21% were great blue herons, and 13% were great egrets. Because numbers reported killed per year represented less than 3% of the continental breeding numbers for each species the authors concluded that the level of legal killing did not adversely affect population sizes of these birds, and Christmas bird-count data showed no evidence of killing affecting numbers of birds present in the region. However, this study did not provide a reliable measure of increase in mortality rate of birds within the states where the killing occurred, and made no allowance for the numbers killed without permits.

Numbers of great cormorants in north-west Scotland have certainly declined in recent decades whereas in every other part of Europe their numbers have been increasing (Lloyd et al. 1991). It is likely, though far from proven, that the decrease in their numbers in north-west Scotland is a direct result of the killing of large numbers of great cormorants at salmon farms; best estimates suggest that 1600 great cormorants were killed each year at Scottish fish farms during the 1980s only a small proportion of these being killed legally under permit (Carss 1994).

Some common eiders are shot by mussel farmers in Scotland, and some are drowned as a result of becoming entangled in anti-predator nets set around mussel farms. However, numbers of common eiders in Scotland are increasing in all areas except Shetland (where deaths of ducks associated with mussel farming have been negligible up to now), and there is no indication from census data that the rate of increase has been noticeably reduced by the mortality associated with mussel farming in other parts of Scotland (Ross and Furness 2000).

If it is difficult to establish the impact of, or even the extent of predator control by aquaculturalists in the United States or Scotland, it is far more difficult to assess the situation in parts of the world where the lobby for wildlife protection is less strong and there is little monitoring of bird or aquatic mammal populations.

In addition to the impact of lethal control measures, non-lethal measures may affect wildlife. In this case the effects are probably minor and mainly involve impacts on local distribution and behaviour rather than on population size. Non- lethal scaring measures regularly used in the aquaculture industry include shooting with blanks, use of gas cannons,

other acoustic deterrents, scarecrows, chasing by powerboat, flashing lights and pyrotechnics. Regular scaring of birds from aquaculture sites may increase their energy needs through increasing the time they have to spend flying, and may reduce their longer term foraging rates. Sea ducks in areas with extensive mussel farming show higher rates of vigilance than ducks in areas without mussel farms, and respond more rapidly (by flying away) when approached by boat (Ross and Furness 2000). This relates to the frequent habit of farmers to chase sea ducks away from mussel farms by powerboat. Birds learn to be more cautious in places where they are subject to such harassment.

5.6 Impacts on birds of the harvest of mussel spat

Mussel farming often relies on the harvest of wild mussel spat to establish cultures of mussels on ropes or on selected intertidal or subtidal plots. Removal of natural spat can be very extensive and can influence food availability for specialist predators of mussels (Kaiser et al. 1998). It is difficult to estimate the importance of mussel spat harvest for dependent wildlife. In many areas the quantity of spat is so large that harvesting some may have little or no influence on subsequent biomass of natural mussel stocks in the region. However, there is one well-documented case where bird populations have been severely affected by mussel spat harvest and mussel farming, combined with fisheries for other molluscs that might have provided alternative prey. In the Wadden Sea, common eiders and Eurasian oystercatchers occur in hundreds of thousands during winter, and feed predominantly on mussels and cockles. These resources are subject to heavy fishery harvest as well as collection of mussel spat for subtidal mussel farming, despite the fact that the Dutch Wadden Sea has been declared a wetland of international importance as a Ramsar site, a Biosphere Reserve, and under the EC Wild Birds Directive and EC Habitats Directive. Mussel spat stock assessment is carried out prior to harvest, and in years of spat scarcity, intertidal areas are now closed to harvesting in order to provide for the food requirements of protected bird populations (Smaal and Lucas 2000). However, in 1990, mussel seed collection led to a near-complete stock depletion, at the same time as harvesting of mature cultivated mussels reduced adult stocks to a very low level. Unprecedented thousands of common eiders and Eurasian oystercatchers died that winter and numbers in the Wadden Sea fell and have remained lower than in the 1970s-80s. Many surviving common eiders moved out of the Wadden Sea and established a new pattern of feeding on another mollusc species, Spisula, available in deeper North Sea waters. Continued harvesting of mussel spat and contraction of the area of mussel beds into smaller areas of protected mussel farms, together with fisheries exploiting Wadden Sea cockles and North Sea Spisula, was followed in winter 1999/2000 by another mass mortality of common eiders, with over 21,000 birds starving to death along the Wadden Sea coastline (Camphuysen et al. ms submitted).

5.7 Impacts of industrial fishing on seabirds

Industrial fishing, to harvest small fish for production of feed for aquaculture, is an indirect, but important, influence of the aquaculture industry on the environment (Naylor et al. 2000). Not only has aquaculture production been increasing, but there has also been a trend towards intensification of aquacultural systems. A particularly rapid increase has occurred in the use of aquafeed in production of predatory fish and crustacea. Aquaculture has tended to ‘feed up the food chain’. This trend has been most pronounced in prawn culture, staple freshwater fish culture and luxury marine fish culture in countries such as China, Indonesia, the Philippines and India. Globally, the use of artificially compounded feeds (‘aquafeeds’) to increase production of farmed finfish and crustacea has increased at a rate in excess of 30% per year for the last few years. Production of around 3 million tonnes of farmed fish and crustacea in 1995 required about 1.5 million tonnes of fish meal and oil, manufactured from over 5 million tonnes of pelagic fish (wet weight). By 2000, nearly 10 million tonnes of pelagic fish was being used in aquafeeds, and this increase is projected to continue. These pelagic fish are harvested by ‘industrial fisheries’, where the entire catch is destined for reduction to fish meal and oil rather than for direct human consumption. The EU is a major importer of global production of fish meal. Most industrial fisheries harvest from stocks of abundant, small, shoaling, pelagic fish such as anchovies, sandeels, capelin, sprats or juvenile herring. Such fish are also food for many predatory fish that are commercially important for human consumption fisheries, as well as supporting many marine mammals and seabirds. Hence concern has been raised over potential for competition between industrial fisheries, commercially important human consumption fisheries, and wildlife conservation interests

The proportion of the global catch of industrial fisheries that is used for aquafeeds has been increasing very rapidly, from 10% in 1988 to 17% in 1994, and 33% in 1997. This gives several causes for concern. The rapid increase in requirement for fish meal and oils could not be met by proportional increases in industrial fish landings, since most major industrial fisheries are fully exploited. By comparison with relatively slowly increasing industrial fish catches, global production of soya has doubled in the last ten years. This has led to increasing prices for fish meal and fish oil whereas soya meal and oil prices have remained relatively constant; this provides an increasing incentive to replace fish with soya in feeds where this is possible.

Figure 5.2. Sandeel landings from the North Sea each year from 1961 to 1995. From Furness (1999).

Even the current levels of industrial fishing may not be sustainable. For example, Peruvian anchovy catches drop considerably in El Nino years. North Sea sandeel catches may only be sustainable as long as stocks of predatory fish remain greatly depleted (Furness 1999). Capelin catches may only remain high while cod stocks that feed on those capelin remain depleted. Collapse of the Barents Sea capelin stock during the 1980s seems to have been due predominantly to very high capelin mortality as a result of rapid increases in cod recruitment but with an additional impact of industrial fishing on the capelin stock (Gjøsæter 1997). It has also been argued that industrial fisheries may have adverse effects on the rest of the food web of which the industrial stocks are a fundamental component because industrial fishery catches can be very large. For example, the North Sea sandeel fishery has grown very rapidly over the last three decades to become the largest single species fishery in the North Sea (Figure 5.2).

Figure 5.3. Breeding performance of black-legged kittiwakes in relation to numbers of sandeels at Shetland. From Furness (1999).

Industrial fisheries might deprive top predators of their food, or may alter energy Flow within a food web to change the balance between fish stocks. Interactions between industrial fisheries and other parts of the ecosystem have been most intensively studied in the North Sea (sandeel fishery), Norway (herring fishery) and in the Barents Sea (capelin fishery). In the case of North Sea sandeels, many seabirds, marine mammals and predatory fish feed predominantly on sandeels in summer when these fish become available in the upper layers of the sea. We know much more about seabird feeding on sandeels than about marine mammal or predatory fish. Ecological theory predicts that some types of seabirds will be much more vulnerable to reductions in food-fish abundance than others. Empirical data from Shetland, where sandeel abundance fell to dramatically low levels in the mid-1980s, support theoretical predictions (Furness and Tasker 2000). One of the species expected to respond most strongly is the black-legged kittiwake. Breeding success of black-legged kittiwakes does indeed correlate with sandeel stock density, both in the North Sea, and in Shetland and over the range of sandeel abundances recorded in these years, the relationship between breeding success and log sandeel abundance is essentially linear (Figure 5.3). The North Sea sandeel fishery was closed from January 2000 in one small area of the North Sea where black-legged kittiwake breeding success had been poor for several seasons following large harvests of sandeels, on the basis that black-legged kittiwake performance represents an indicator of the availability of sandeels to top predators in general. However, black-legged kittiwake breeding success has been high in most North Sea colonies, and breeding numbers have increased alongside the growing industrial fishery (Furness 1999). Why has this been possible? It seems that reductions in stocks of predatory fish have more than compensated for the growing industrial fishery. Predatory fish, especially mackerel and gadoids, are by far the largest consumers of sandeels, while the needs of seabirds and marine mammals are very much less (Figure 5.4).

Figure 5.4. Percentages of the annual take of the North Sea stock of sandeels attributable to particular consumer groups; North Sea mackerel stock, east Atlantic mackerel stock known as ‘western mackerel’, gadoids (primarily whiting, haddock and cod), all other piscivorous fish plus seals, the North Sea industrial fishery, and seabirds. Quantities were estimated by bioenergetics modelling plus data on stomach contents of fish and diet composition of seabirds and seals. Data from ICES (1997).

The implication of this is that changes in abundance of predatory fish probably influence sandeel availability to seabirds and seals more than the industrial fishery does. A large industrial fishery may be compatible with healthy populations of seabirds and marine mammals in the North Sea providing predatory fish stocks remain depleted.

In Norway, long-term studies of Atlantic puffin and black-legged kittiwake breeding ecology show strong correlations between breeding success and herring abundance (Anker-Nilssen and Aarvak 2001, Anker-Nilssen unpubl.). 0-group herring abundance explains 89% of the variation in fledging success of Atlantic puffins in the largest colony in Norway, but also 84% of annual variation in adult survival rate of Atlantic puffins, indicating a surprisingly strong influence of herring abundance on adult survival rate which is generally believed to be much less sensitive to food abundance than is reproductive success. Furthermore, the clearly sigmoidal nature of these effects is demonstrated (Anker-Nilssen and Aarvak 2001). Performance remains fairly consistent down to a certain threshold herring abundance, rapidly falling to a low level when herring abundance falls below the threshold value. The extent to which the interannual variations in Norwegian herring abundance are due to effects of industrial fisheries is a matter of debate, but the strong influence of herring abundance on Atlantic puffin and black-legged kittiwake breeding success and on Atlantic puffin survival imply that effects of industrial fishing on herring abundance will feed through to impacts on these seabirds if herring abundance is caused to decline below the threshold level.

In the Barents Sea, stocks of cod and herring have been heavily exploited for human food consumption, and capelin are harvested by an industrial fishery. The capelin stock collapsed in the mid-1980s and again in the early 1990s. These collapses were largely due to high predation rates by cod, resulting from exceptionally large cod year classes, but exacerbated by the industrial fishery for capelin (Bogstad and Mehl 1997, Gjøsæter 1997). The consequence for seabirds and marine mammals was dramatic. Huge numbers of starving seals from the arctic invaded Norwegian coastal waters in search of food. Almost 90% of common guillemots in the Barents Sea starved to death in winter 1986–87 because they could not find alternative food in the absence of capelin (Vader et al. 1990, Barrett and Krasnov 1996). Despite these catastrophes, there are common features between the Barents Sea and North Sea ecosystems. In both, predatory fish are by far the biggest consumer of the food fish, with the industrial fishery and marine mammals taking less, and seabirds less again (Furness and Tasker 1997, Mehlum and Gabrielsen 1995). In both, fluctuations in predatory

fish stocks appear to influence food fish availability to wildlife more than the industrial fishery does. However, both cases show that top predators such as seabirds and marine mammals are vulnerable to alterations in ecosystem structure, whether induced by natural variation or by fisheries.

Elsewhere, interactions between industrial fisheries, marine mammals and seabirds have not been quantified in detail. However, the loss of millions of seabirds from the Peruvian coast is a well-known example where the industrial fishery for anchoveta seems to have reduced food availability to the birds, thereby inhibiting their populations from recovering after crashes induced by El Nino events (Duffy 1983).

A trend in aquaculture has been to reduce the quantity of fish meal and oil going into the production of a unit of aquaculture produce. Improvements in the feeding efficiency of aquaculture systems have been taking place, so that the amount of feed wasted in intensive systems has been reduced. This is important in reducing farm waste pollution impacts, but higher conversion efficiency also reduces the requirement for industrial fishing products. At present, most aquafeeds are over-formulated as nutritionally complete diets regardless of stocking density and natural food availability, and this requires adjustment to further reduce wastage. Another trend that may mitigate increased requirements for aquafeeds is alteration of aquafeed composition to contain less fish meal and oil. Industrial fish protein can to some extent be substituted by soya protein (Thomson 1990) though this could lead to concerns over use of genetically modified organisms in the human food chain. Fish oil can similarly be substituted by vegetable oil. Specific limiting nutrients can be added to try to compensate for chemical compositional differences between fish and other ingredients. At the moment there is much research by commercial aquafeed companies to investigate these alternatives and the suitability of altered feeds for aquaculture production and product quality. IFOMA has estimated that use of aquafeed will more than double between 2000 and 2010 (Table 5.1). Despite reductions in the proportions of fish meal and oil in aquafeed, the quantities of these constituents needed to support this growth are anticipated to increase by about 30% over that decade (Table 5.2).

Although FAO estimate that about 25 million tonnes of fish are discarded worldwide each year, mechanisms and facilities to collect these and to convert them to fish meal and oil are rarely available, and it would not be desirable to encourage development of a market for discards as the aim of management should be to reduce to a minimum the amounts of discards generated. Furthermore, many contaminants are stored in fish livers and accumulate to higher concentrations in larger and older fish, so that contaminant problems might arise if discards and offal from continental shelf and enclosed sea fisheries were substantial contributors to fish meal. Most industrial fish are short lived and occur in upwelling regions where pollution is negligible. While it seems that some changes that reduce dependence on fish meal and oils may be practical, it is likely that the overall trend for the foreseeable future will be greater demand for fish meal and oil in aquaculture rather than a reduction, and it is probable that inclusion of discards and offal will represent only a small fraction of future aquafeed production. To the extent that industrial fisheries remove food required by seabirds or deplete prey fish stocks, they may adversely affect seabird populations. If, as seems to be the case, fishing down the food chain results in a reduction in total mortality imposed on prey fish stocks, then adverse impacts of industrial fisheries seem more likely in upwelling food chains, where fishing down the food chain tends not to be evident. Industrial fisheries on shelf fish stocks may be less likely to have adverse effects on seabirds because they tend to harvest from stocks of food fish that are subject to reduced mortality because their main (fish) predators have been depleted.

Table 5.1. Projections of aquaculture production by species groups and estimated requirements for aquafeeds (IFOMA).

Species Production in Estimated Predicted % estimated to % projected to Aquafeed use Aquafeed use Aquafeed Aquafeed 1996 (‘000 t) production in production in be on aquafeed be on aquafeed per tonne per tonne required in 2000 required in 2010 2000 (‘000 t) 2010 (‘000 t) in 2000 in 2010 produced in produced (‘000 t) (‘000 t) 2000 expected in 2010

Carp 11,504 13,983 36,268 25 50 2 1.5 6,991 27,000

Tilapia 801 974 2,526 40 60 2 1.5 779 2,106

Shrimp 1,034 1,034 1,684 80 90 1.8 1.6 1,489 2,425

Salmon 644 876 1,569 100 100 1.2 0.8 1,051 1,255

Bass, etc1 629 856 1,394 60 80 1.8 1.5 923 1,670

Trout 400 450 733 100 100 1.3 0.8 585 586

Catfish 330 371 604 85 90 1.6 1.4 505 761

Milkfish 364 379 462 40 75 2.0 1.6 303 554

Eel 216 216 263 80 90 2.0 1.2 346 284

Other marine 60 105 650 100 100 1.2 0.9 126 585 fish

Total 15,982 19,244 46,153 13,098 37,226 1. Bass, bream, yellowtail, grouper, jacks and mullets.

Table 5.2. Predicted requirements for fish meal and oil for use in aquafeeds in 2010 compared with present use (data from IFOMA).

Species % Fish Predicted % % Fish Predicted Fish meal Fish meal Fish oil Fish oil meal in fish meal in oils in % Fish required required in required required in feed in feed in feed in oils in in 2000 2010 (‘000 t) in 2000 2010 (‘000 t) 2000 2010 2000 feed in (‘000 t) (‘000 t) 2010 Carp 5 2.5 1 0.5 350 675 70 135 Tilapia 7 3.5 1 0.5 55 74 8 11 Shrimp 25 20 2 3 372 485 29 73 Salmon 40 30 25 20 454 377 283 251 Bass, etc1 45 40 20 15 415 668 185 251 Trout 30 25 15 20 176 147 88 117 Catfish 3 - 1 1 15 - 5 8 Milkfish 12 5 3 2 36 28 10 11 Eel 50 40 5 10 173 114 17 28 Other 55 45 10 12 69 263 13 70 marine fish Total 2,115 2,831 708 955

1 Bass, bream, yellowtail, grouper, jacks and mullets.

5.8 References

Accord, B. R. 1995. Cormorant management and responsibilities: United States Department of Agriculture. Colonial Waterbirds 18: 231–233.

Anker-Nilssen, T. and Aarvak, T. 2001. The population ecology of puffins at Røst. Status after the breeding season 2000. NINA Oppdragsmelding 684: 1–40. (in Norwegian with English abstract).

Avery, M. L., Eiselman, D. S., Young, M. K., Humphrey, J. S. and Decker, D. G. 1999. Wading bird predation at tropical aquaculture facilities in central Florida. North American Journal of Aquaculture 61: 64–69.

Barrett, R. T. and Krasnov, J 1996. Recent responses to changes in fish stocks of prey species by seabirds breeding in the southern Barents Sea. ICES Journal of Marine Science 53: 713–722.

Belant, J. L., Tyson, L. A. and Mastrangelo, P. A. 2000. Effects of lethal control at aquaculture facilities on populations of piscivorous birds. Wildlife Society Bulletin 28: 379–384.

Blackwell, B. F., Dolbeer, R. A. and Tyson, L. A. 2000. Lethal control of piscivorous birds at aquaculture facilities in the northeast United States: effects on populations. North American Journal of Aquaculture 62: 300–307.

Bogstad, B. and Mehl, S. 1997. Interactions between Atlantic cod (Gadus morhua) and its prey species in the Barents Sea. pp. 591–615 In Proceedings Forage Fishes in Marine Ecosystems. Alaska Sea Grant College Program AK-SG-97– 01, Fairbanks.

Brugger, K. E. 1995. Double-crested cormorants and fisheries in Florida. Colonial Waterbirds 18: 110–117.

Carss, D. N. 1994. Killing of piscivorous birds at Scottish fin fish farms, 1984–87. Biological Conservation 68: 181– 188.

Costa-Pierce, B. A. 1998. Preliminary investigation of an integrated aquaculture-wetland ecosystem using tertiary- treated municipal wastewater in Los Angeles County, California. Ecological Engineering 10: 341–354.

Dorr, B., Clark, L., Glahn, J. F. and Mezine, I. 1998. Evaluation of a methyl anthranilate-based bird repellent: toxicity to channel catfish Ictalurus punctatus and effect on great blue heron Ardea herodias feeding behaviour. Journal of the World Aquaculture Society 29: 451–462.

Duffy, D. C. 1983. Environmental uncertainty and commercial fishing: effects on Peruvian guano birds. Biological Conservation 26: 227–238.

Erwin, R. M. 1995. The ecology of cormorants: some research needs and recommendations. Colonial Waterbirds 18: 240–246.

Fleury, B. E. and Sherry, T. W. 1995. Long-term population trends of colonial wading birds in the southern United States: the impact of crayfish aquaculture on Louisiana populations. Auk 112: 613–632.

Furness, R. W. 1999. Does harvesting a million metric tons of sand lance per year from the North Sea threaten seabird populations? pp. 407–424 In Ecosystem Approaches for Fisheries Management. University of Alaska Sea Grant College Program. AK-SG-99–01, 1999, Fairbanks.

Furness, R. W. and Tasker, M. L. 1997. Seabird consumption in sand lance MSVPA models for the North Sea, and the impact of industrial fishing on seabird population dynamics. pp. 147–169 In Proceedings Forage Fishes in Marine Ecosystems. Alaska Sea Grant College Program AK-SG-97–01, Fairbanks.

Furness, R. W. and Tasker, M. L. 2000. Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance and identification of key areas for sensitive seabirds in the North Sea. Marine Ecology Progress Series 202: 253–264.

Genard, M., Masse, J., and Rigaud, C. 1993. Experimental approach to the predation by piscivorous birds in extensive water aquaculture. Bulletin Fr. Pech. Piscic. 329, 231–243.

Gjøsæter, H. 1997. The Barents Sea capelin stock (Mallotus villosus): a brief review. pp. 469–484 In Proceedings Forage Fishes in Marine Ecosystems. Alaska Sea Grant College Program AK-SG-97–01, Fairbanks.

Glahn, J. F. and Brugger, K. E. 1995. The impact of double-crested cormorants on the Mississippi Delta catfish industry: a bioenergetics model. Colonial Waterbirds 18: 168–175.

Glahn, J. F., Rasmussen, E. S., Tomsa, T. and Preusser, K. J. 1999a. Distribution and relative impact of avian predators at aquaculture facilities in the northeastern United States. North American Journal of Aquaculture 61: 340–348.

Glahn, J. F., Tomsa, T. and Preusser, K. J. 1999b. Impact of great blue heron predation at trout-rearing facilities in the northeastern United States. North American Journal of Aquaculture 61: 349–354.

Hemre, G.-I. and Sandnes, K 2000. By-catch and offal from the herring industry – performance of Atlantic salmon as concerns growth, feed utilisation and fillet quality. ICES CM 2000/P:02.

ICES, 1997. Report on the Working Group on Multispecies Assessment. ICES CM1997/Assess:16.

Kaiser, M. J., Laing, I., Utting, S. D. and Burnell, G. M. 1998. Environmental impacts of bivalve mariculture. Journal of Shellfish Research 17: 59–66.

King, D. T. 1996. Movements of double-crested cormorants among winter roosts in the Delta Region of Mississippi. Journal of Field Ornithology 67: 205–211.

Kushlan, J. A. 1997. The conservation of wading birds. Colonial Waterbirds 20: 129–137.

Lloyd, C., Tasker, M. L. and Partridge, K. 1991. The status of seabirds in Britain and Ireland. Poyser, London, 355 pp.

McKay, H., Furness, R., Russell, I., Parrott, D., Rehfisch, M., Watola, G., Packer, J., Armitage, M., Gill, E. and Robertson, P. 1999. The assessment of the effectiveness of management measures to control damage by fish-eating birds to inland fisheries in England and Wales. Central Science Laboratory, York.

Mehlum, F. and Gabrielsen, G. W. 1995. Energy expenditure and food consumption by seabird populations in the Barents Sea region. pp. 457–470 In Skjoldal, H. R., Hopkins, C., Erikstad, K. E. and Leinaas, H. P. (eds.) Ecology of fjords and coastal waters. Elsevier, Amsterdam.

Milne, H. and Galbraith, C. 1986. Predation by eider ducks on cultivated mussels. Final report to DAFS and HIDB, University of Aberdeen. 161pp.

Mooney, N. 1998. Status and conservation of raptors in Australia’s tropics. Journal of Raptor Research 32: 64–73.

Moravec, F., Vidal Martinez, V. M., Vargas Vazquez, J., Vivas Rodriguez, C., Gonzalez Solis, D., Mendoza Franco, E., Sima Alvarez, R. and Guemez Ricalde, J. 1997. Helminth parasites of Epinephelus morio (Pisces: Serranidae) of the Yucatan Peninsula, southeastern Mexico. Folia Parasitologica 44: 255–266.

Mott, D. F. and Boyd, F. L. 1995. A review of techniques for preventing cormorant depredations at aquaculture facilities in the southeastern United States. Colonial Waterbirds 18: 176–180.

Naylor, R. L., Goldburg, R. J., Primavera, J. H., Kautsky, N., Beveridge, M. C. M., Clay, J., Folke, C., Lubchenco, J., Mooney, H. and Troell, M. 2000. Effect of aquaculture on world fish supplies. Nature 405: 1017–1024.

Nelson, J. G. 1993. Conservation and use of the Mai Po Marshes, Hong-Kong. Natural Areas Journal 13: 215–219.

Nettleship, D. N. and Duffy, D. C. 1995. Cormorants and human interactions: an introduction. Colonial Waterbirds 18: 3–6.

Pitt, W. C., and Conover, M. R. 1996. Predation at Intermountain West fish hatcheries. Journal of Wildlife Management 60: 616–624.

Price, I. M. and Nickum, J. G. 1995. Aquaculture and birds: the context for controversy. Colonial Waterbirds 18: 33–45.

Ross, B. P. and Furness, R. W. 2000. Minimising the impact of eider ducks on mussel farming. University of Glasgow, Glasgow. 54pp.

Russell, I. C., Dare, P. J., Eaton, D. R. and Armstrong, J. D. 1996. Assessment of the problem of fish-eating birds in inland fisheries in England and Wales. Directorate of Fisheries Research, Lowestoft. 130pp.

Smaal, A. C. and Lucas, L. 2000. Regulation and monitoring of marine aquaculture in the Netherlands. Journal of Applied Ichthyology 16: 187–191.

Thomson, C. J. 1990. The market for fish-meal and oil in the United States 1960–1988 and future prospects. California Cooperative Ocean Fisheries Investigation Report 31, 124–131.

Trapp, J. L., Dwyer, T. J., Doggett, J. J. and Nickum, J. G. 1995. Management responsibilities and policies for cormorants: United States Fish and Wildlife Service. Colonial Waterbirds 18: 226–230.

Ulenaers, P. and van Vessem, J. 1994. Impact of great crested grebes (Podiceps cristatus L) on fish ponds. Hydrobiologia 280: 353–366.

Vader, W., Barrett, R. T., Erikstad, K. E. and Strann, K. B. 1990. Differential responses of common and thick-billed murres to a crash in the capelin stock in the southern Barents Sea. Studies in Avian Biology 14: 175–180.

6 FURTHER REVIEW OF THE CONTENTS ON THE DATABASE ON SEABIRD DIET COMPOSITION

The diet database resulted from a survey of 921 studies or datasets, providing detailed information of prey taken by 38 species of seabirds, divers (loons), grebes and seaduck in 20 ICES subregions and 4 NAFO areas. The database is by no means complete and some predator species and ICES areas are covered better than others. Best covered to date are Atlantic puffin (155 studies), common guillemot (80), great skua (75), and northern fulmar (68). Some 161 studies were not assigned to any specific ICES or NAFO subregion, while 237 studies were in subregion IVa, 153 in IVb, 69 in I, 49 in IVc and VIa, and 47 in IIb. The data are also heavily biased to the breeding season, with 534 out of 921 datasets referring to that period and a further 31 studies being related to the ‘summer’ period (covering 27 species in total). Some 65 datasets referred to the pre-nesting period (17 species), 90 to the post-breeding season (23 species), 120 to the winter period (21 species) and 81 studies were not assigned (20 species). A large update of the database, covering particularly the cormorant and gull families has been prepared, but has yet to be formally incorporated.

7 WHAT QUESTIONS CAN WE TRY TO ANSWER DURING CONCURRENT MEETINGS WITH OTHER WORKING GROUPS?

This question was also addressed during the 2000 Working Group meeting. The Group reviewed its thinking in 2000, and decided that had not changed its mind since then. It therefore repeats its advice.

The group considered that this initiative by the Oceanography Committee was very promising. While links with areas of marine science of some of our sister working groups might be viewed as esoteric, there was clear promise in working with WGOH, WGZE and WGCCC. This Working Group can provide long-term datasets and insights on seabird abundance, seabird range changes, seabird breeding success and seabird diet. It would be interested in any other long- term datasets that might be of use in interpreting trends in these datasets.

In 1998, the Working Group addressed a term of reference “review evidence for decadal scale variations in seabird distributions, populations sizes, reproduction and food habits and evaluate the extent to which these may be linked to the North Atlantic Oscillation and other physical cycles”. When the 1998 report (ICES CM 1998/C:5) was under review, the relevant section of the report was (rightly, in hindsight) criticised as being naïve as it had little input from oceanographers. The concurrent meetings proposed for 2002 appear to be an ideal occasion to correct this fault, and we hope that oceanographic colleagues could help with this. The question might indeed be expanded to “Can linkages be found between time series of changes in seabird and oceanographic parameters?”. From our review of the 2000 terms of reference to the Oceanography Committee groups it would appear that WGOH would be most relevant to this question.

There have been attempts to link at-sea distribution of seabirds with hydrographic features on the Northwest European shelf by several authors. It might prove instructive to review these attempts and consider whether there were any general findings, and to identify any areas for further research. It would appear that the expertise of the WGOH would be most relevant.

8 RECOMMENDATIONS

8.1 Proposal for next meeting

The Working Group on Seabird Ecology makes the following proposals:

1) The Working Group on Seabird Ecology [WGSE] (Chair: R. Furness ) will meet at ICES Headquarters from 8–11 or 15–18 March 2002 to: a) Compile a first model of food consumption by seabirds for the entire ICES area; b) Compile population estimates for breeding seabirds in the ICES area, preferably divided by ICES fishing areas; c) Add further information to the review of status of and threats to seabirds in the North Sea; d) Review methods for assessing seabird vulnerability to oil pollution; e) Review the effects of windfarms on seabirds; f) Work with the ICES Secretariat to provide summaries of seabird information via the ICES website.

8.1.1 Supporting information

Priority: This is the only work being carried out by ICES in relation to marine birds. If ICES wishes to maintain its profile in this area of work, then the work of the Group must be regarded as of high priority. Scientific a) The Working Group has been modelling consumption for a number of years, Justification: with a view to developing a model of the whole ICES area in due course. The information should be of interest to other ICES Working Groups, as well as to OSPAR and HELCOM. b) The most recent agreed and published figures for breeding numbers in the ICES area derive from the mid 1980s. A compilation in 2002 will allow the results of major recent censuses to be incorporated. c) The review conducted in 2001 had to use some information on status that is more than ten years old. WGSE is aware of further surveys and analysis that will be carried out in 2001. This new information should be incorporated in any status statement. WGSE started, but were unable to complete, a review of threats to seabirds in the North Sea at their 2001 meeting. WGSE proposes to work inter-sessionally to complete this review in time for agreement at its meeting. d) A number of methods exist to assess the sensitivity of birds to marine oil pollution; WGSE proposes to review these methods in order to help attempts to agree international standards. e) Proposals to develop marine sites for windfarms have grown very rapidly in recent years. Several studies of their effects on marine birds are under way, and now would be a very opportune moment to review these studies to see if any wider conclusions can be drawn. f) The group wishes its work to be better known within ICES and in the wider world. Relation to The above will help achieve the following within the initial ICES strategic plan Strategic Plan Goal 1. Develop a challenging core science programme to fulfil the ICES Mission. Goal 2. Provide sound, credible, timely, and understandable advice that is relevant to today’s and future societal needs. Goal 5. Raise public understanding of marine ecosystems and their relevance to society. Objective 1. Understand the physical, chemical, and biological functioning of marine ecosystems. Objective 2. Understand and quantify human impacts on the marine environment, including living marine resources. Objective 3. Develop the scientific basis for sustainable use and protection of the marine environment, including living marine resources.

Objective 4. Provide advice on the sustainable use and protection of the marine environment, including living marine resources. Objective 5. Co-ordinate and support interdisciplinary and international marine science programmes. Objective 6. Broaden the diversity of the scientists that participate in ICES activities. Objective 11. Make the scientific products of ICES more accessible to the public

Resource The ICES Headquarters is a good working environment. Since all active members Requirements: of the group are at present funded outside core funding (some are privately funded) within the Member Countries, meeting over a weekend will minimise travel costs of members. If the meeting started on a Friday and finished on a Monday, beneficial interaction with the Secretariat would still be possible. This is a Core Activity.

Participants: The present members of the Group should be able to achieve most of the above objectives, however some may not be able to attend through lack of funding. Funding for these members from Member Countries would be very welcome. In addition, Oceanography Committee (and ourselves) consider that the Group still has a very “northern” outlook, and we make the following suggestions for nominations to remedy this: David Gremillet (France), Mark Bolton (Portugal). We have lacked expertise on seaduck and shorebirds and we make the following suggestions of specialists to help here: Theunis Piersma (Netherlands), Herman Höttker (Germany). Olof Olsson (Sweden) would add valuable experience from Sweden and the Baltic.

Secretariat The usual excellent support from the Secretariat will be appreciated. Facilities:

Financial: No financial implications.

Linkages to Both ACFM/ACME would find the consumption model of use, either in assessing Advisory the environmental needs of seabirds or in estimating effects of seabirds on fish Committees: stocks.

Linkages to other The Working Group is keen to continue the process of integration of seabird Committees or ecology into the workings of ICES. We look forward to possible concurrent Groups working with sister Groups under the Oceanography Committee umbrella. WGSE thinks that a similar process would be productive for groups working under other Committees. Linkages to other The circumpolar seabird working group (CSWG) of CAFF is interested in the Organisations review of methods for assessing seabird vulnerability to oil.

8.2 Proposal for a Cooperative Research Report

An ICES Cooperative Research Report (possible title “Seabirds as Monitors of the Marine Environment”) be compiled and edited by Mark Tasker and Bob Furness, and be published by ICES. The Cooperative Research Report will be based on Chapters 3–5 of ICES CM 2001/C:05 (Report of the Working Group on Seabird Ecology, ICES Headquarters, March 2001), Chapters 2–3 from ICES CM 2000/C:04 (Report of the Working Group on Seabird Ecology, Wilhelmshaven, Germany March 2000) and Chapter 3 from ICES CM 1999/C:5 (Report of the Working Group on Seabird Ecology, ICES Headquarters, March 1999). The chapters from the earlier reports have already been reviewed and approved by the Chairs of the Oceanography and Marine Habitats Committees. The estimated number of pages is 70.

8.2.1 Supporting Information

Priority: WGSE has produced two Cooperative Research Reports in the past based on the more substantial chapters of its working group reports. WGSE is keen to continue its efforts to raise the profile of seabird work within ICES. The section on ecological quality objectives in the 2001 working group report is of particular interest and relevance at present as it derives from a request from OSPAR to ICES.

Scientific The proposed ICES Cooperative Research Report will represent a synthesis of Justification: recent work by WGSE on monitoring the effects of human activities on seabirds, and the usefulness of such monitoring to those attempting to reduce these effects by managing such activities.

Relation to The above will help achieve the following within the initial (2000) ICES strategic Strategic Plan plan Goal 5. Raise public understanding of marine ecosystems and their relevance to society. Objective 1. Understand the physical, chemical, and biological functioning of marine ecosystems. Objective 2. Understand and quantify human impacts on the marine environment, including living marine resources. Objective 3. Develop the scientific basis for sustainable use and protection of the marine environment, including living marine resources. Objective 4. Provide advice on the sustainable use and protection of the marine environment, including living marine resources. Objective 11. Make the scientific products of ICES more accessible to the public

Resource Publication of this material as a CRR will cost about xxxxDKK. The material in Requirements: the report is already available in electronic files, so no specific additional costs are foreseen.

Participants: About 1 week of work will be needed between the two editors

Secretariat About xxx of the services of Secretariat Professional and General Staff will be Facilities: required

Financial: Publication costs

Linkages to ACME has reviewed and commented on some of the proposed chapters. ACE has Advisory commented on the EcoQOs Committees:

Linkages to other Committees or Groups

Linkages to other Monitoring of seabirds is of interest to OSPAR (through BDC), the North Sea Organisations Ministerial Process, the Wadden Sea Trilateral Agreement

8.3 Chair

The current chair (Mark Tasker, UK) has chaired three meetings of the Working Group. The group unanimously nominated Professor Bob Furness (UK) to be chair for the next three meetings, pending the approval of the Oceanography Committee.

8.4 Request to other groups for information

The Working Group still requires information on the energy density of seabird prey species from other ICES Working Groups. WGSE is further interested in variation in energy density including both temporal and geographic as well as such factors as length, age and stage. The Group noted that information on discarded fish was equally as important as naturally caught fish. A list of some of the more important prey species in which we are interested was provided in our 2000 report (ICES CM 2000/C:04 Report of the Working Group on Seabird Ecology, Wilhelmshaven, Germany March 2000) Groups that may have members with relevant expertise or knowledge include: SGDEEP, SGBHSM, HAWG, SGDBI, WGBFAS, NWWG, WGNPBW, WWGNSDS, AFWG, WGEEL, WGSSDS, WGMHSA, WGNSSK, WGZE, WGCEPH, WGMMPD, SGNEPH, SGEF, WGCRAN, SGCRAB, and SBCAR. In addition, those Groups charged with planning surveys might consider whether it would be possible to gain information on energy density of marine species as an adjunct to the surveys.

8.5 Proposal for a Mini-Symposium

WGSE wishes to co-sponsor a mini-symposium on Physical/Biological coupling and trophic transfer to predators at the 2002, or 2003 Annual Science Meeting. Physical processes at a wide variety of spatial and temporal scales are becoming recognized as important for the profitable foraging of many groups of organisms from zooplankton to fish to seabirds and marine mammals. At the larger spatial and temporal scales, places where these transfers are concentrated may be hotspots of particular concern for conservation of marine resources. We wish to explore these ideas over a wide range of organisms and spatial scales.

We wish to at least have papers on copepods, on jellyfish, and a couple each in fish, birds and mammals. Some of the recent remote sensing work on mammals, birds and fish could usefully be presented. One further area of interest would be in contrasting responses of predators to regions of enhanced production as opposed to areas with mechanical aggregation of prey. It would therefore be useful to have papers on bio/physical coupling and production and on mechanical aggregation.

Proposed conveners of the Mini-symposium from WGSE are George Hunt (USA) and Simon Greenstreet (UK). Further co-conveners will be sought from other disciplines.

ANNEX 1 – NAMES AND ADDRESSES OF PARTICIPANTS

Name Address Telephone Telefax E-mail Mark. Tasker Joint Nature Conservation +44 1224 655 701 +44 1224 621 488 [email protected] (Chair) Committee Dunnet House 7, Thistle Place Aberdeen AB10 1UZ United Kingdom Tycho Anker-Nilssen NINA +47 73 80 14 43 +47 73 80 14 01 [email protected] Tungasletta 2 NO-7485 Trondheim Norway Peter H. Becker Institut für Vogelforschung +49 4421 96890 +49 4421 968955 [email protected] An der Vogelwarte 21 D-26386 Wilhelmshaven Germany Thierry Boulinier Laboratorie d'Ecologie +33 144 27 3213 +33 144 27 3516 [email protected] CNRS - UMR 7625 Universite Pierre & Marie Curie 7, Quai St Bernard 75005 Paris France Gilles Chapdelaine Service Canadien de la +1 418 649 6127 +1 418 648 6475 [email protected] Faune Environment Canada 1141, route de l'Eglise Ste-Foy, Quebec G1V 4H5 Canada Bob W. Furness Institute of Biomedical and +44 141 330 3560 +44 141 330 5971 [email protected] Life Sciences The University of Glasgow Graham Kerr Building Glasgow G12 8QQ United Kingdom Mick Mackey Coastal Resources Centre +353 21 490 4287 +353 21 490 4289 [email protected] Old Presentation Building University College Cork Western Road Cork, Ireland Norman Ratcliffe Royal Society for the +44 1767 680 551 +44 1767 492 365 [email protected] Protection of Birds Cons. Science Department The Lodge Sandy, Bedfordshire SG19 2DL United Kingdom Jim Reid Joint Nature Conservation +44 1224 655 702 +44 1224 621 488 [email protected] Committee Dunnet House 7, Thistle Place Aberdeen AB10 1UZ United Kingdom Richard Veit Biology Department +1 718 982 3862 +1 718 982 3852 [email protected] College of Staten Island 2800 Victory Boulevard Staten Island NY 10314, USA

ANNEX 2 – SCIENTIFIC NAMES OF SPECIES USED IN THIS REPORT

Galapagos penguin Spheniscus mendiculus Red-throated diver Gavia stellata Black-throated diver Gavia arctica Great northern diver Gavia immer Great crested grebe Podiceps griseigena Red-necked grebe Podiceps grisegena Wandering albatross Diomedea exulans Northern fulmar Fulmarus glacialis Cory’s shearwater Calonectris diomedea Manx shearwater Puffinus puffinus Short-tailed shearwater Puffinus tenuirostris European storm-petrel Hydrobates pelagicus Leach’s storm-petrel Oceanodroma leucorhoa Northern gannet Morus bassanus Great cormorant Phalacrocorax carbo Double-crested cormorant Phalacrocorax auritus European shag Phalacrocorax aristotelis Brown pelican Pelecanus occidentalis Black-crowned night heron Nycticorax nytcticorax Great egret Ardea alba Great blue heron Ardea herodias Grey heron Ardea cinerea Brent goose Branta bernicla Common shelduck Tadorna tadorna Greater scaup Aythya marila Common eider Somateria mollissima Long-tailed duck Clangula hyenalis Black scoter Melanitta nigra Velvet scoter Mellanitta fusca Common goldeneye Bucephala clangula Red-breasted merganser Mergus serrator Goosander Mergus merganser Osprey Pandion haliaetus Common quail Cotornix cotornix Eurasian oystercatcher Haemotopus ostralegus Ringed plover Charadrius hiaticula Kentish plover Charadrius alexandrius European golden plover Pluvialis apricaria Grey plover Pluvialis squatarola Northern lapwing Vanellus vanellus Red knot Calidris canutus Sanderling Calidris alba Dunlin Calidris alpina Common snipe Gallinago gallinago Black-tailed godwit Limosa limosa Bar-tailed godwit Limosa lapponica Eurasian curlew Numenius arquata Common redshank Tringa totanus Common greenshank Tringa nebularia Ruddy turnstone Arenaria interpres Arctic skua Stercorarius parasiticus Great skua Stercorarius skua Mediterranean gull Larus melanocephalus Little gull Larus minutus Bonaparte’s gull Larus philadelphia Red-billed gull Larus novaehollandiae Black-headed gull Larus ridibundus Mew gull Larus canus Audouin’s gull Larus audouinii Lesser black-backed gull Larus fuscus Herring gull Larus argentatus

Yellow-legged gull Larus cachinnans California gull Larus californicus Great black-backed gull Larus marinus Black-legged kittiwake Rissa tridactyla Gull-billed tern Gelochelidon nilotica Sandwich tern Sterna sandvicensis Roseate tern Sterna dougallii Common tern Sterna hirundo Arctic tern Sterna paradisaea Little tern Sterna albifrons Common guillemot Uria aalge Brunnich’s (thick-billed) guillemot Uria lomvia Razorbill Alca torda Black guillemot Cepphus grylle Little auk Alle alle Atlantic puffin Fratercula arctica Common raven Corvus corax