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EMF - electrical cables and their impacts

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Collision risk impacts specific to Indonesia

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Collision risk impacts specific to Indonesia

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Monitoring techniques - anything specific to Indonesia

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Habitat creation and reef effects from infrastructure

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Which seabird species are likely vulnerable to MRE in Indonesia?

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Abstract

Furness, R. W., Wade, H. M., Robbins, A. M. C., and Masden, E. A. 2012. Assessing the sensitivity of seabird populations to adverse effects from tidal stream turbines and wave energy devices. - ICES Journal of Marine Science, 69: .

Tidal turbines and wave energy devices may affect seabird populations through collision mortality, disturbance and habitat loss. Given the pressures to harness tidal and wave energy, especially in Scottish waters, there is an urgent need to assess population-level impacts on seabird species. With a lack of deployed devices to monitor in areas of importance for seabirds, our approach uses data from scientific literature on seabird ecology and conservation importance likely to influence population vulnerability to "wet renewables" in Scottish waters. At this stage however, we can only infer likely interactions with tidal and wave devices. We identify black guillemot, razorbill, European shag, common guillemot, great cormorant, divers and Atlantic puffin as the species most vulnerable to adverse effects from tidal turbines in Scottish waters. We identify divers as the species most vulnerable to adverse effects from wave energy devices in Scottish waters. Wave energy devices seem likely to represent a lesser hazard to seabirds than tidal turbines, and both forms of energy capture seem likely to represent a lower hazard to seabirds than offshore wind farms (wind-power plants). The indices developed here for Scottish seabird populations could be applied to populations elsewhere. This approach will help in identifying likely impacts of tidal and wave energy deployments on seabirds, and in optimizing deployment of resources for compulsory environmental monitoring.
Introduction

To meet targets for a reduction in greenhouse gas emissions, the Scottish and UK Governments are encouraging the rapid development of new marine technologies in Scottish waters to generate electricity from tidal and wave power ("wet renewables") ( HM Government, 2010). Many tidal stream turbines resemble wind turbines but designs also include vertical or horizontal axis crossflow turbines, flow augmented turbines (within a duct or shroud), oscillating devices and venture effect devices (see en.wikipedia.org/wiki/Tidal_stream_generator). Most tidal turbines are designed to be pinned to the sea bed well below depths used by shipping. Wave energy devices are usually floating structures that capture wave energy from the bending of joints between linked modules. However, a wide variety of devices may capture wave energy, including devices on the seabed (see en.wikipedia.org/wiki/Wave_power). Tidal and wave energy devices are likely to be deployed in large arrays, though occupying much smaller areas of sea than taken up by offshore wind farms ( ICES, 2010). Scotland has some of the best natural resources in the world in terms of tidal flows and wave climate ( Shields et al., 2009), however, the development of wet renewables may potentially impact seabird populations through the effects of collision, disturbance, and/or habitat loss ( ICES, 2010; Langton et al., 2011). Since seabirds are typically long-lived and produce only small numbers of offspring that have a low probability of surviving to breeding age, direct mortality of adult seabirds has a far more pronounced impact on population dynamics than effects influencing breeding success ( Furness and Monaghan, 1987). As a result, the hazards of additional mortality to adult seabirds greatly outweigh indirect influences resulting from disturbance or habitat loss affecting breeding productivity.

As well as holding some of the best tidal and wave energy resources, Scotland also holds internationally important populations of many seabird species ( Mitchell et al., 2004; Forrester et al., 2007). Many seabirds in Scotland breed within Special Protection Areas (SPAs) and so are protected by law (Scottish Habitats Regulations), potentially creating a conflict between energy generation and seabird conservation (a figure showing SPAs in Scotland and details of designated species can be found at SNH Sitelink http://gateway.snh.gov.uk/sitelink/ but note that there are over 40 sites already designated as SPAs for seabirds around Scotland, many of which are close to the key sites for wave and tidal stream energy development). There is a need to assess which seabird species are most likely to be affected by wet renewables, so that research and monitoring can focus on those species in locations where their populations overlap with wet renewable deployments ( ICES, 2010). It is also important that species unlikely to be affected by interactions with wet renewables can be excluded, in an objective and scientifically appropriate manner, by regulators, developers and consultants. Impacts of tidal turbines and wave energy devices on seabirds are however largely unknown at present because there have not yet been enough deployments to study ( Witt et al., 2012). Nevertheless, an assessment can be made on the basis of knowledge of seabird ecology and inference of the effects of these devices on the physical environment and on lower trophic level organisms i.e. prey of seabirds ( WWT Consulting, 2010; ABP Marine Environmental Research, 2011). OSPAR (Oslo and Paris Convention; the mechanism by which 15 European governments with western coasts and catchments protect the marine environment) recently requested guidance on this issue from the International Council for the Exploration of the Sea (ICES), and the ICES response was summarized as "impacts of wave, and particularly tidal stream devices, have the potential to be significant for some groups of organisms. It is important that the results of thorough monitoring of early deployments of wave and tidal stream devices are published and used to guide the management of subsequent developments" ( ICES, 2010). However, assessment of potential impacts is required imminently to assist in the legal process of Environmental Impact Assessment (EIA) in relation to proposed development, especially where such developments may affect seabird populations in SPAs.

Fraenkel (2006) suggested that diving seabirds may normally be swept through the blades of a tidal turbine unharmed due to entrainment in the flow of water. However, this assumes that seabirds flow passively in the water rather than moving across or against the current. It is very unlikely that seabirds simply move passively with flowing water, and all the available evidence indicates that diving seabirds move actively through the water, and often swim against the current (e.g. Lovvorn and Jones, 1991; Holm and Burger, 2002; Daunt et al., 2003; Heath et al., 2006; Watanuki et al., 2006; Harding et al., 2009; Langston, 2010). For example, common eiders Somateria mollissima always dive against the current and normally surface upstream of their entry point ( Heath et al., 2006). Seabirds that forage on the sea floor (i.e. on benthic prey) may be particularly vulnerable to collision with tidal turbine blades, especially where birds have travelled some distance across the sea floor before they ascend to the surface. This may bring them, unexpectedly, into the swept area of a turbine blade, from below. It is evident that seabirds able to dive deep are more likely to come into contact with tidal turbines, as are those seabirds that make particular use of tidal races as foraging habitat. Seabirds that are less able to avoid underwater hazards are more likely to be killed by such structures, and seabirds that forage over small areas of sea close to the coast are more likely to be affected by tidal turbines than seabirds that forage over large areas of pelagic habitat. It has also been suggested that the slow turbine speeds relative to the manoeuvrability of diving bird species would make the risk of seabird mortality very low ( Awatea, 2008). However, a typical seabird swimming speed is of the order of 1.5 ms −1 ( Wanless et al., 1988, 1993, 1997, 1998; Halsey et al., 2006a, b; Heath et al., 2006; Ribak et al., 2008; Thaxter et al. 2010) and a tidal turbine blade tip turning at 15 r.p.m. would be moving faster than this ( ICES, 2010) and so potentially be difficult for a bird to avoid. ICES (2010) also highlight that "alterations in patterns of turbulence may affect the feeding behaviour of some seabirds, particularly terns". In addition, wave energy convertors have the potential to alter water column and sea bed habitats, and by changing the wave climate/environment may cause changes some distance from the installation, however due to the infancy of the industry, empirical evidence is lacking. It is against this background of a lack of scientific evidence from research studies into the impacts of wave and tidal devices on seabirds, that there is a need to evaluate likely impacts of these new technologies on seabirds. Wherever possible it should be based on the detailed knowledge of relevant aspects of seabird ecology and behaviour and mindful of the absence of detailed information on the devices and their deployment. Here we review evidence for likely impacts on seabirds, and construct indices assessing the relative vulnerability of seabird species' populations to impacts of tidal turbines and of wave energy devices.

Methods and Results

This review firstly considers tidal turbines and impacts they may have on seabirds, and secondly considers wave energy devices and their impacts. Desholm (2009) argued that in order to prioritize bird species for assessment of the impact of mortality at wind farms, it is possible to consider just two criteria; proportion of the population at risk and demographic elasticity (essentially represented by adult survival rate). Birds with high proportions of their populations coming into contact with devices and with high adult survival rates will be more severely impacted than birds with small proportions of their populations coming into contact with devices and with low natural survival rates. While that approach has the benefit of great simplicity, it does not take into account the fact that some kinds of birds are more, or less, likely to be affected as a consequence of their species-specific ecology or behaviour. This review therefore follows the approach developed by Furness and Tasker (2000), and successfully implemented for offshore wind farm hazards to seabirds in the southern North Sea by Garthe and Hüppop (2004). The method scores a number of factors considered to influence risk at the population level and wherever possible, the scores allocated to species for each factor are evidence-based, with relevant references cited where appropriate. Where the evidence base is especially limited however, the set of scoring criteria and provisional scores for seabird species, which are based on the available evidence taken from the reviewed literature, have been circulated to a group of appropriate experts for moderation (details in Acknowledgements). This was intended to ensure that the final criteria and scores have wide consensus support from stakeholders, including seabird ecologists, and conservationists. The list of seabird species includes true seabirds, wintering sea ducks and grebes, and the white-tailed eagle Haliaetus albicilla. Seabirds excluded from the list were the few species considered not to be likely to interact with wet renewables in Scottish waters either because their distribution was entirely coastal (such as red-breasted mergansers Mergus serrator), or because their numbers in Scottish waters were very low or limited to occurring over very short time periods.

Conservation status factors

We have scored similar factors to those presented by Garthe and Hüppop (2004), but we have adjusted the factors to reflect conservation importance of seabird populations in a Scottish rather than southern North Sea context. The index developed by Garthe and Hüppop (2004) included nine factors, of which three represented conservation status of the species and six represented aspects of the hazard that devices were considered to represent, based on aspects of the ecology of each species. A similar approach has been followed here though four factors are used as measures of conservation status: status in relation to the Birds Directive, percentage of the biogeographic population that occurs in Scotland, adult survival rate, and UK threat status.

Birds Directive status

The Birds Directive is a European Union directive adopted in 2009 to protect European wild birds and their habitats, in particular through the designation of Special Protection Areas (SPAs). The Birds Directive gives extremely powerful protection to birds, particularly those listed in Annex 1. Species listed in Annex 1 of the Birds Directive were given a score of 5 while species qualifying as "Migratory species" but not on Annex 1 were scored 3. Remaining species score 1. These scores (Supplementary Table 1) reflect aspects of conservation importance, but are not necessarily optimal for guidance regarding consenting risk.

Percentage of the biogeographic population in Scotland

The percentage of the biogeographic population (usually based on continuous distribution of the relevant subspecies, taken as the North Atlantic or European or Palearctic population as seems appropriate for particular species) occurring in Scotland was assessed from Forrester et al. (2007), or by comparing the population estimate in Forrester et al. (2007) with the biogeographic population estimates given in del Hoyo et al. (1992, 1996). Scores were allocated as: 1 (<1%), 2 (1-4%), 3 (5-9%), 4 (10-19%), or 5 (≥20%) (Supplementary Table 1). Since this metric may vary seasonally, we used the highest seasonal score for each species.

Adult survival rate

Published data on adult survival rate (which are robust data for most seabird species) were included as a factor to reflect the vulnerability of species to any increase in mortality (due to "wet renewables") above natural mortality. Species with low rates of adult survival will tend to be less vulnerable to additional mortality than species with high annual survival. Data were taken from the scientific literature ( del Hoyo et al. 1992, 1996; Garthe and Hüppop, 2004; Glutz von Blotzheim and Bauer,1982; Saether, 1989), from individual species studies, or estimated from data for closely related species. Where several estimates were available, preference was given to more recent studies, and studies in the UK, since survival rates in populations of the same species may sometimes differ between geographical regions. Adult survival rates were classified on a scale from 1 to 5 according to Garthe and Hüppop (2004): 1 (adult survival <0.749), 2 (adult survival 0.75-0.799), 3 (0.80-0.849), 4 (0.85-0.899), 5 (adult survival >0.90) (Supplementary Table 1).

UK threat status

This factor reflects both threat and conservation status of the species in the UK, as given by Eaton et al. (2009) in "Birds of Conservation Concern 3" (BOCC3). For some species, the classification in BOCC3 differs from that in the previous assessment (BOCC2), and these changes are also taken into account here, given the implications of changes in status. Scores were allocated as follows: 1 (green in BOCC2 and BOCC3), 2 (amber in BOCC2 and green in BOCC3), 3 (green in BOCC2 and amber in BOCC3), 4 (amber in BOCC3 and BOCC2), 5 (red in BOCC3) (Supplementary Table 1).

Vulnerability factors for tidal turbines

Scores for the various vulnerability component factors are arranged on a scale of 1-5, where 5 is a strong anticipated negative impact. It is assumed that these individual factor scores can then be summed to give a total for each species that ranks species according to the likely conservation concern with regard to these developments. Seven factors are scored, representing negative effects of tidal turbines on seabirds or sensitivities of the ecology of seabird species: drowning risk, mean and maximum diving depth, benthic foraging, use of tidal races for foraging, feeding range, disturbance by ship traffic, and habitat specialization. Other factors, such as impacts of anti-fouling paints on structures or chemical spillages associated with the structures, were considered not to represent a significant threat to seabirds.

Drowning risk

Seabird species vary in their risk of drowning. For example some species appear to be particularly prone to getting stuck in nets and traps, while others avoid such hazards more successfully. Differences among species are likely to be caused by a range of features, including species' morphology, feeding ecology, and behaviour. It is well known that juvenile birds are often more prone to such mortality than adults. For example, ring recoveries of juvenile shags Phalacrocorax aristotelis occur not infrequently in lobster pots, whereas adult shags are rarely trapped in this way ( Galbraith et al., 1981). Scoring species on this factor is difficult, since it is impossible to obtain quantitative data on such risk across species, but there are published studies reviewing the causes of mortality of seabirds which identify drowning through entanglement with underwater structures and its prevalence in certain birds (such as sea ducks and divers; Zydelis et al., 2009). For surface-feeding seabirds the risk of encountering tidal turbines is clearly very low. For diving seabirds we have reviewed literature to identify species most at risk, and have used the peer review process (expert judgement) to moderate scores. Risk is scored from extremely low (score 1) to moderate (score 5) (Supplementary Table 2).

Mean and maximum diving depth

Seabirds capable of diving to depths where tidal turbines will be deployed, and regularly doing so, will presumably be at greater risk of colliding with these structures. Depth deployment of tidal turbines is uncertain at present, and varies with design but is typically 30-50 m below sea surface ( Aquatera, 2010). Mean and maximum diving depths of seabirds have been recorded for many species, predominantly by deployment of data loggers on breeding seabirds. Scores were allocated as follows: score 1 (surface feeders with maximum diving depth no more than 1 m); score 2 (regularly dive to 2 or 3 m but have a maximum diving depth of no more than 5 m); score 3 (regularly dive to 5 m but rarely below 20 m); score 4 (regularly dive to 20 m but rarely below 40 m); score 5 (regularly dive to 30 m and deeper). These depth categories were chosen to spread the species out among the five categories, and to clearly separate species likely to attain depths where tidal turbines are deployed from those unable to access such depths. Where data differ between studies, we gave greater weighting to more recent studies which tend to use instrumentation rather than inference i.e. inferred depth from time spent (Supplementary Table 3).

Benthic foraging

Benthic foraging seabirds are more likely to interact with tidal turbines than seabirds that do not forage on benthic prey. This score ranges from 1 (<5% benthic foraging); 2 (5% ≤ benthic foraging < 20%); 3 (20% ≤ benthic foraging < 40%); 4 (40% ≤ benthic foraging < 70%); 5 (70% ≤ benthic foraging < 100%). Again, these categories were selected to spread species out over the five scores (Supplementary Table 4).

Use of tidal races for foraging

There have been very few studies of the use of high tidal flow areas by foraging seabirds, and most of the few published studies relate to seabirds in the North Pacific. However, Slater (1976) showed that common guillemots Uria aalge, in Orkney displayed a tidal rhythm in foraging activity during the early part of the breeding season, but not during chick-rearing. He suggested that this tidal rhythm indicated a higher prey capture rate during low tide periods or possibly during the rising tide, and that this might be a feature particularly prominent in Orkney due to the high flow through the archipelago and the Pentland Firth. Arctic terns Sterna paradisaea and common terns S. hirundo in the Wadden Sea also forage selectively at stages of the tide and in geographical locations with relatively faster flowing (1 m/sec) shallow (<10 m) water ( Schwemmer et al., 2009), because this apparently increases their prey capture rates ( Schwemmer et al., 2009). However, the tidal flow rates reported by Schwemmer et al. (2009) are relatively low in comparison to areas under consideration for deployment of tidal turbines (usually in excess of 4 m/sec). Scores are based on these cited references and others wherever possible, moderated by peer assessment, and are assigned to spread species out over the five categories. The scores ranged from 1 (habitat strongly avoided) to 5 (preferred habitat) (Supplementary Table 5).

Feeding range

Breeding seabirds are "central place foragers" and so are constrained to return to the central place (the nest site). In winter and during migration periods, seabirds are considerably less constrained and some species of seabirds may travel over enormous distances, but some seabirds even in winter are limited by the need to return to a safe nocturnal roost site, or to spend the night out of water (e.g. cormorants). Although the distribution of predictable feeding hotspots may influence habitat quality for seabirds, species with short feeding ranges will be more likely to be affected by the placement of renewable energy devices than seabirds with greater foraging ranges. The latter species can pass by areas with tidal turbines with minimal loss of foraging opportunity. Seabirds with short foraging ranges may lose higher proportions of their available foraging area if displaced by the presence of devices. We have classified scores as: score 1 (mean range generally over 90 km, and maximum generally over 150 km); score 2 (mean range 20-90 km and maximum around 100-150 km); score 3 (mean range 10-20 km and maximum around 50-80 km); score 4 (mean range 5-10 km and maximum around 20-50 km); score 5 (mean range less than 5 km and maximum generally less than 20 km). Where the maximum and the mean range values reported in the literature fell into different scores based on these criteria, we gave higher weight to the mean values. Where several estimates were available in the literature and these fell into different score bands, we gave less weighting to estimates that were in review publications rather than based on original data, less weighting to estimates reported in unpublished reports or reports that appeared not to have been peer reviewed, less weighting to older literature, and less weighting to estimates derived indirectly from data such as time spent away from the nest combined with estimated flight speed (and more weighting to data derived from direct measures such as deployment of GPS loggers on breeding birds). Where no data could be found for particular species, scores were estimated from the scores allocated to closely related species with similar ecology (Supplementary Table 6).

Disturbance by ship traffic

Seabird species differ in their reaction to the ship traffic that occurs during deployment and maintenance of tidal turbines. This behaviour relates in part to the general responsiveness of species to disturbance, and in part to specific responses to ships, although the latter can vary as a result of habituation. In the context of offshore wind farms, Garthe and Hüppop (2004) presented a similar vulnerability factor based on both ships and helicopters as disturbances. For tidal turbine arrays however, it is likely that ships will be used for maintenance work rather than helicopters, so the index here is only in relation to ship disturbance. It is known that alcids can be disturbed by boats hundreds of metres away ( Ronconi and Clair, 2002; Bellefleur et al., 2009), that divers are especially sensitive to approaching boats more than 1 km away ( Schwemmer et al., 2011), and amongst the sea ducks, scoters are particularly vulnerable to disturbance by boats ( Kaiser et al., 2006; Schwemmer et al., 2011). Scores were allocated as: 1 (little or no response of birds to vessels passing close by), 2 (slight avoidance at short range), 3 (low to moderate flush distance, or moderate avoidance at short range), 4 (moderate to high flush distance), 5 (birds often flushed at long range (1000 m or more) and moderate to high short-term loss of foraging opportunity due to disturbance) (Supplementary Table 7).

Habitat specialization

Seabirds vary in the range of habitats they use, for example relating to water masses and frontal systems and whether they use these as specialists or generalists. This score classifies species into categories from 1 (tend to forage over large marine areas with little known association with particular marine features) to 5 (tend to feed on very specific habitat features, such as shallow banks with bivalve communities, or kelp beds). Where available, scores presented by Garthe and Hüppop (2004) were used. Scores for other species were based on foraging ecology described in single species studies in the literature, or from standard handbook descriptions. Literature indicates many cases of species showing limited flexibility in feeding habitat. For example, common eiders, long-tailed ducks Clangula hyemalis and common scoters Melanitta nigra are dependent on shallow feeding grounds with shellfish banks ( Garthe, 2006). Species scoring 4 or 5 are more likely to be adversely affected by loss of habitat if tidal turbines or wave energy devices are placed within areas that they would otherwise use for foraging (Supplementary Table 8).

Assessing an overall score for species' vulnerability to tidal turbines

Garthe and Hüppop (2004) computed a risk index that summed four related factors and divided the sum by four, and multiplied that by the sum of two other factors divided by two. This recognized that the last two factors related to different aspects from the first four. They then multiplied for each species the answer from this formula by the conservation importance score for the species. Ranking species by the final index value provides a simple way to identify those populations that appear to be most vulnerable. A similar procedure is used here.

Of the various risk factors scored, the use of tidal races as a foraging habitat seems to be especially important in determining overall vulnerability. The diving ability of species appears also to be highly important, while the other five factors may be placed as of similar, but lower importance. To recognize this, the overall index value for each species has been computed as:

The index value could therefore range up to 25. We divided index scores into 5 categories: very low vulnerability (score ≤ 1), low vulnerability (1 < score ≤ 2), moderate vulnerability (2 < score ≤ 5), high vulnerability (5 < score ≤ 10), and very high vulnerability (10 < score ≤ 25). These categories are arbitrary, but are designed to be precautionary (in setting a very wide range of scores in the top category of very high vulnerability and very narrow ranges of scores in the two lowest categories) and to discriminate between high and low groups of species (Table 1).

Vulnerability factors for wave energy devices

We have included seven factors. Of these, five are scored on a 1 to 5 scale (risk of collision mortality due to structures, exclusion from foraging habitat, disturbance by structures, disturbance by ship traffic, and flexibility in habitat use), with 5 representing high vulnerability or impact. The final two factors (benefit from roost platform, and benefit from fish attraction device effects or biofouling) are scored on a negative scale from 0 to -2 (0 representing no effect and -2 representing a small benefit for birds of that species). Other factors, such as impacts of anti-fouling paints on structures or chemical spillages associated with the structures, were considered not to represent a significant threat to seabirds so are not considered here.

Risk of collision mortality due to structures

Some seabirds may be at risk of injury or death from colliding with wave energy devices, either in flight or while swimming or diving. This score classifies species into categories from 1 (minimal risk of mortality) to 5 (moderate risk of mortality) (Supplementary Table 9). Given the nature of wave energy devices, even a score of 5 on this factor would probably represent a relatively low risk compared to risks such as entanglement in netting.

Exclusion from foraging habitat due to behavioural constraints

Wave energy devices might prevent some seabirds from foraging in important habitat. This may be because the seabirds are unable to land or take off readily where devices are present in the water, because other birds have been attracted into the area and affect their foraging, or because they need to spend time avoiding the devices rather than searching for food. The impact may be trivial however for seabirds which have long foraging ranges and a wide diversity of habitats in which they can feed. For example, divers need open water for landing and taking off, and may be unable to land in areas where devices block a descent flight onto the water. The score classifies species into categories from 1 (minimal exclusion) to 5 (moderate exclusion from foraging habitat) (Supplementary Table 10).

Benefit from roost platform

Under relatively calm sea conditions, wave energy devices may provide some seabirds with a resting platform. For some seabirds such an opportunity could extend their potential foraging area. For example, great cormorants Phalacrocorax carbo and shags need to return to shore to dry their plumage after a foraging bout. Having resting sites at sea could allow these birds to exploit areas further from shore that would otherwise be uneconomical for birds to commute to from the shore. Such situations have been reported, for example in the case of cormorants in the Baltic Sea which now extend their foraging distribution further offshore by roosting on the structures of the offshore wind farm at Nysted. The score for this factor classifies species into categories from 0 (no significant benefit likely) to -2 (moderate likelihood of species gaining benefit from opportunity to roost on structures) (Supplementary Table 11). The choice of -2 as the extreme and the use of only three categories recognizes that this effect is likely to be relatively minor at a population level.

Benefit from Fish Attraction Device (FAD) effect or biofouling

Wave energy devices will probably provide shelter for small fishes and so are likely to act as a fish attraction device (FAD) ( Rountree, 1990; Castro et al., 2001; Løkkeborg et al., 2002; Wilhelmsson et al., 2006; Langhamer and Wilhelmsson, 2009). They may also represent surfaces onto which biofouling organisms will settle. Aggregations of fish under wave devices, and attached animals could attract foraging seabirds by providing locally high densities of prey. This may explain the reported attraction of some seabirds to structures such as oil platforms ( Baird, 1990; Wiese et al., 2001). The score for this factor classifies species into categories from 0 (no significant benefit likely) to -2 (moderate likelihood of species gaining benefit from opportunity to feed on a locally high density of fish attracted to devices) (Table S12).

Disturbance by structures

Seabird species differ in their reaction to structures. This behaviour relates in part to the general responsiveness of species to disturbance, and in part to their perception of the hazards represented by structures. This score classifies species into categories from 1 (minimal risk of disturbance) to 5 (moderate risk of disturbance) (Table S13).

Disturbance by ship traffic

Disturbance generated through deployment and/or maintenance of wave energy arrays was considered to be the same as the level of disturbance generated from tidal turbine deployment and/or maintenance. We applied the same scores and score allocations detailed in the tidal turbine assessment.

Habitat specialization

Species that use a wide range of habitats or forage over large areas may not be constrained by reduced availability of a small area around a wave device. In contrast, seabirds that have highly specialized and restricted foraging habitat in small areas where wave devices may be deployed could be prevented from using key habitat for foraging. This score classifies species into categories from 1 (use a wide range of habitats over a large area) to 5 (specialize in using a very limited and predominantly inshore habitat). The same scores are used as in the tidal turbine assessment.

Assessing an overall score for species' vulnerability to wave energy devices

Scores were then grouped into five categories: very high vulnerability (scores above 400), high vulnerability (scores 301-400), moderate vulnerability (scores 201-300), low vulnerability (scores 101-200), and very low vulnerability (scores 0-100) (Table 2). These categories are arbitrary, but are designed to permit species to be labelled into groups that are convenient for developers and regulators.

Key Results

The key results from this assessment are ranked species lists in Table 1 (species ranked by population vulnerability in relation to tidal turbine impacts) and in Table 2 (species ranked by population vulnerability in relation to wave energy device impacts). For tidal turbine impacts, no species fell into the very high vulnerability category (Table 1). Five species fell into the high vulnerability category: black guillemot Cepphus grylle, razorbill Alca torda, European shag, common guillemot, and great cormorant. Five species fell into the moderate vulnerability category: great northern diver Gavia immer, red-throated diver G. stellata, Atlantic puffin Fratercula arctica, black-throated diver Gavia arctica, and little auk Alle alle. The remaining 28 species fell into categories low or very low vulnerability, suggesting that their populations are unlikely to be affected by tidal turbine development. For wave energy devices, no species fell into the categories of very high or high vulnerability (Table 2). Three species (red-throated diver, black-throated diver and great northern diver) fell into the category of moderate vulnerability. A total of 19 species fell into the category of low vulnerability and 16 into very low vulnerability.

Discussion

With rapid development of wet renewables in UK and Scottish waters, there is an urgent need to assess any effects these developments may have on the environment. At present, however, there is a lack of information on the impacts that tidal turbines and wave energy devices may have on seabird populations, which hinders the consenting process for the early developments. Here we have presented an index to assess the vulnerability of seabird populations based on appraisal of detailed scientific literature on aspects of seabird ecology and conservation. The ten species that were identified as moderately or very highly vulnerable to tidal stream turbines should be a focus for monitoring and for research into effects of tidal turbines on seabirds in Scottish waters. The results for wave energy devices suggest that they represent a lesser hazard to seabirds than do tidal turbines, and both types of wet renewables appear to represent a lesser hazard than offshore wind, though to a different set of species (offshore wind collision hazard seems likely to be especially high for large gulls and northern gannets ( Garthe and Hüppop, 2004; Furness and Wade, 2012), species that are predicted to be at low risk from tidal turbines and wave energy devices). From this study it is possible to highlight species such as black guillemot and divers as most likely to be affected by "wet renewable" developments. Although in this paper the focus is on seabird species, in some cases different populations of a species are present at different times of year. Breeding numbers of seabirds in Scotland are well known, but numbers and populations present outside the breeding season may be less certain. Nevertheless, in theory at least, hazard can be assessed separately for breeding populations and for migrants visiting Scottish waters.

During this assessment there were limitations due to the available literature. One such limitation was that data in the BirdLife online database were not clearly attributed to sources and appeared to exaggerate diving depths, especially mean dive depth, compared to most published studies. We also found that some studies of foraging range report mean foraging distance whilst others report the maximum. Where possible, we gave higher importance to reported mean foraging distances than to maximum values. This is partly because maximum values tend to increase with sample size whereas means are not biased in this way. However, maximum foraging ranges of seabird species have been reported in the literature for various species, locations and time periods, more often than mean values have been reported ( Thaxter et al., 2012). It must be remembered that mean and maximum ranges can vary considerably according to environmental conditions. In particular, foraging ranges tend to be short in years with good food supply, but much longer when food is scarce (e.g. Hamer et al., 1993). Ranges can also be much greater when seabirds are nesting in very large colonies ( Hamer et al., 2001). Also, while it is clear that breeding seabirds have a well-defined foraging range from their colony, wintering seabirds and sea ducks have less clearly defined foraging ranges from roosting areas to feeding grounds.

While we have taken the approach of defining risk factors and scoring seabird species according to chosen risk factors, risk levels are likely to change in relation to a wide range of additional variables. Risk will vary seasonally, in relation to weather conditions, age, experience and breeding status of individual birds, and probably for a variety of other reasons, some of which are understood by ecologists and some of which are probably not. Scores allocated are averages for each species, but within-species variation should not be ignored. For example, seabird at-sea activity levels tend to be considerably higher in summer when birds are breeding than they are during winter ( Markones et al., 2010). High energetic demands of breeding and increased travelling activity and foraging will potentially increase risk of interactions with tidal turbines and wave energy devices. On the other hand, while breeding, seabirds are central-place foragers, tied to areas in the vicinity of their breeding colonies. This could result in rates of interaction with tidal turbines and wave energy devices varying seasonally depending on whether these devices are close to colonies (in which case interactions may predominantly occur during the breeding season) or in areas distant from colonies (in which case interactions may occur predominantly during seabird migration periods, or in winter). At-sea distributions and behaviours of breeding seabirds are becoming quite well known, meaning we have a detailed knowledge of the distributions and sizes of seabird colonies, and deployment of data loggers is starting to provide information on the foraging behaviour of breeding adults. The distributions and behaviour of non-breeding (immature) seabirds are however poorly known, and the youngest seabirds may be most vulnerable to hazards because they lack experience. Juvenile European shags occasionally drown by becoming trapped in lobster pots; adult shags hardly ever die in this way ( Galbraith et al., 1981). A similar age-related variation in risk applies in the context of drowning in fishing nets ( Murray et al., 1994). These differences may relate in part to the distributions of these age classes of birds, but is more likely a consequence of the inexperience of juvenile birds. Similar differences in relation to hazards posed by tidal turbines and wave energy devices are likely to affect juvenile seabirds in particular.

Suitability of a Vulnerability Index approach

Desholm (2009) identified two weaknesses in the approach we have used. The first is the fact that different factors are measured on different scales. It does have to be acknowledged that it is impossible to add up a mortality rate and a percentage of biogeographic population in a common currency. It is because factors are measured on different scales that the index classifies species into five levels (scores) for each factor, and then combines scores. Because we are trying to compare "apples and oranges" these comparisons and scores are using a small number of categories and essentially ranking species in order to identify those with extreme characteristics on each factor. This clearly does need to be done with caution given that different factors are measured in different units. The assumption being made is that all of these factors influence risk, and therefore that a species scoring high on all factors will be at highest risk and a species scoring low on all factors will be at lowest risk. It would be unwise to assume that species A, scoring high on the first factor but low on a second, had exactly the same risk as species B, scoring low on the first factor but high on the second. Scores for each species should be seen as an indication of the likely overall picture, and not as an exact quantitative measure on a scale. The issue of correlations between factors was also raised by Desholm (2009) who pointed out that there were correlations between nearly one-third of pairwise comparisons of factors in their study of seabirds and offshore wind farm risk. Similar correlations may exist between some factors scored in this study. For example, it would be surprising if the percentage of benthic food in the diet did not correlate with diving depth, simply because seabirds that cannot dive have little or no access to benthic prey. Such correlations need not be a problem. For example, in using biometrics to discriminate between males and females of a particular seabird species with limited sexual dimorphism, it is usually more successful to combine several linear measurements (head, bill depth, tarsus length etc.) rather than use a single metric. This would be particularly true if each measurement differed slightly between the sexes, but with considerable individual variation and measurement error. Then combining several measures reduces the effects of measurement error. For our scoring, there is considerable uncertainty in the allocation of scores for individual species for each factor, so combining several factors to give an overall index may be better than relying on a measurement for a single factor, especially if that measurement is inaccurate.

Limitations of data

A draft version of the factors and species-scores was sent to seabird experts for comment. Most reviewers suggested no change to the factors used, and no change to most scores. Most of the reviewers felt that between one and four out of the 456 scores for risk factors might be altered slightly, but were content with over 99% of the allocated scores. Therefore the scores presented in this paper have broad agreement from a diverse group of relevant experts in seabird ecology and conservation, selected for their particular interest in wet renewables. None of the reviewers questioned scoring in the assessment of conservation importance of species. That reflects the high quality of data on Scottish seabird population sizes and conservation status, and the strongly quantitative and evidence-based approach used in scoring. Nevertheless, within the scoring factor "Birds Directive status" we felt that it would be useful also to consider the proportion of the Scottish population of each species that is protected within the SPA network, a statistic of direct relevance to consenting risk. Unfortunately, such data are not readily available for Scotland. In the SPA review (Stroud et al., 2001) such a statistic is considered at a Great British and biogeographic level, but those data are not calculated at a Scottish level, and are now also somewhat out of date. This score could therefore be improved if a database of current numbers of seabirds in SPAs in Scotland could be established, and kept up to date.

The evidence base for scoring species risk factors is much less secure, and the relatively consistent consensus view of seabird ecologists is based on detailed knowledge of seabird ecology, but on a lack of evidence from deployed tidal and wave energy devices. It would not be too surprising, therefore, if at least a few of these consensus views turn out in future to be inaccurate. It is, therefore, important to treat the results of this project with caution, and it should be an objective to continuously update the assessments made in this report with data that will eventually become available as the wet renewables industry develops. This view is closely in agreement with the conclusions reached by ICES (2010) in their advice on wet renewables environmental impacts given to OSPAR.

Applications of findings to impact assessments

Despite the relatively high uncertainty over species-specific responses to tidal devices and to wave energy devices, there is a very strong consensus in the published literature that these wet renewables technologies are unlikely to represent as great a hazard to seabirds as posed by offshore wind farms ( Awatea, 2008; Inger et al., 2009; Aquatera, 2010; ICES, 2010; Grecian, 2010; Langton et al., 2011; Witt et al., 2012). The relatively low risk to seabirds from wet renewables also contrasts strongly with the high impact on seabird populations resulting from depletion of fish stocks by global fisheries ( Karpouzi et al., 2007; Cury et al., 2011), and potentially from climate change ( Mackas et al., 2007; Beaugrand et al., 2009; Quillfeldt et al., 2010). In this context of changing numbers of seabirds as a result of changes in fish stocks and fisheries, zooplankton populations, climate change and other pressures, the influences of wet renewables on seabird populations are inevitably going to be very difficult to measure. This review represents a small step towards identifying the seabird species in Scottish waters that should be the main focus of concern for the regulator (Marine Scotland) the statutory advisor (Scottish Natural Heritage), developers and their consultants, in relation to deployments of tidal turbines and wave energy devices. We strongly recommend that this assessment be updated as more studies provide relevant information, and that monitoring and research particularly targets the species in the top parts of the lists in Tables 1 and 2. This review does not inform on site-specific issues, and in the context of EIA should be seen as assisting with scoping and with cumulative impacts assessment. Clearly each individual development will need to consider site-specific issues and the local community of seabirds in that area.

Supplementary data

Supplementary material is available at the ICESJMS online version of the manuscript.

Funding

This study was jointly funded by Scottish Natural Heritage and MacArthur Green Ltd.

Acknowledgements

We are very grateful to a large number of seabird ecologists who provided advice on the factors and the species scores for factors, and suggested useful literature to review:Prof. Stuart Bearhop (University of Exeter), Dr John Calladine (BTO Scotland), Dr Keith Hamer (University of Leeds), Prof. Mike Harris (CEH Edinburgh), Martin Heubeck (SOTEAG, Shetland), Dr Liz Humphreys (BTO Scotland), Dr Beth Scott (University of Aberdeen), Dr Chris Thaxter (BTO), Prof. Paul Thompson (University of Aberdeen), Dr Steve Votier (University of Plymouth), Prof. Sarah Wanless (CEH Edinburgh), Dr Steve Newton (Birdwatch Ireland), and Dr James Grecian (University of Glasgow). We thank Dr Roel May and an anonymous reviewer for helpful comments on an earlier draft.

References

Author notes

# data[].attributes.attachment_link.title
Assessing the sensitivity of seabird populations to adverse effects from tidal stream turbines and wave energy devices

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Furness, R. W., Wade, H. M., Robbins, A. M. C., and Masden, E. A. 2012. Assessing the sensitivity of seabird populations to adverse effects from tidal stream turbines and wave energy devices. - ICES Journal of Marine Science, 69: . Tidal turbines and wave energy devices may affect seabird populations through collision mortality, disturbance and habitat loss.

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Changes in flow, both local and far-field, affecting habitat and connectivity

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Changes in flow, both local and far-field, affecting habitat and connectivity

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Depth of knowledge of MRE development in Indonesia - what do we know and what don't we know?

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Depth of knowledge of MRE development in Indonesia - what do we know and what don't we know?

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Ecologically significant changes in flow and wave climate caused by energy extraction

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Ecologically significant changes in flow and wave climate caused by energy extraction

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Exclusion zones providing opportunities for spatial fisheries management

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Exclusion zones providing opportunities for spatial fisheries management

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Displacement of impacts from other activities such as fishing

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Displacement of impacts from other activities such as fishing

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What is known about distribution of vulnerable taxa in Indonesian waters?

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What is known about distribution of vulnerable taxa in Indonesian waters?

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Knowledge of cumulative impacts particularly if lots of small-scale developments rather than a few larger developments

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Knowledge of cumulative impacts particularly if lots of small-scale developments rather than a few larger developments

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disaster as a context - other ecological changes - what's the baseline? volcanoes, earthquakes, tsunamis etc

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disaster as a context - other ecological changes - what's the baseline? volcanoes, earthquakes, tsunamis etc

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Economic and engineering uncertainties associated with disasters

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Economic and engineering uncertainties associated with disasters

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more opportunities for local communities and engagement - SDGs

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more opportunities for local communities and engagement - SDGs

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Potential for MRE to play a role in coastal protection?

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Potential for MRE to play a role in coastal protection?

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Co-developments, e.g. MRE and aquaculture

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Co-developments, e.g. MRE and aquaculture

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Small-scale MRE as an enabling technology for remote coastal communities, e.g. allowing more efficient resource use in fisheries through access to refrigeration

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Small-scale MRE as an enabling technology for remote coastal communities, e.g. allowing more efficient resource use in fisheries through access to refrigeration

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temperature - changes from higher temperature and speed of biofouling etc

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temperature - changes from higher temperature and speed of biofouling etc

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is the ecology a priority in Indonesia or is more consenting / planning / policy more immediate. what is the priority from an MRE perspective in Indonesia

# data[].attributes.subject
is the ecology a priority in Indonesia or is more consenting / planning / policy more immediate. what is the priority from an MRE perspective in Indonesia

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Link/assess scale of development/device with risk from disaster

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Link/assess scale of development/device with risk from disaster

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High tech monitoring system vulnerability to disaster

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High tech monitoring system vulnerability to disaster

# data[].attributes.headline
Modelling of flow, temperature, sediment transport , turbulence

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Modelling of flow, temperature, sediment transport , turbulence