Potential consequences of discard reform for seabird communities

Authors


Correspondence author. E-mail: stephen.votier@plymouth.ac.uk

Summary

  1. Upcoming reform of the European Union (EU) Common Fisheries Policy will be the biggest change in European fisheries management for a generation. A central plank of this reform is a proposed ban on discards, to aid the creation of economically and environmentally sustainable fisheries. This, together with a global trend for declining discards, may have unforeseen knock-on consequences for the large number of scavenging seabirds that consume this plentiful subsidy.

  2. Discards have shaped many aspects of seabird foraging, distribution and population dynamics. Here, we review these effects and consider the potential for both negative and positive impacts of discard reforms for seabirds, with particular focus on the EU, and propose recommendations for ongoing research and conservation.

  3. EU seabird scavengers are dominated by a relatively small number of large generalist taxa. Many of these occur at globally significant numbers within the EU, but may be able to buffer a decline in discards by switching to feed on alternative foods.

  4. A discard ban may have negative consequences by creating a food shortage for scavenging birds. Some species may offset this by feeding more on other birds, with potentially negative population-level impacts, or by moving into novel environments.

  5. Benefits of a discard ban may be a reduction in seabird bycatch in fishing gears, as well as a reduction in populations of large generalist species that currently dominate some seabird communities.

  6. Synthesis and applications. Reform of the Common Fisheries Policy and global discard declines are essential components towards creating sustainable fisheries, but may have both detrimental and beneficial effects on seabird communities. The nature of these impacts is still poorly understood, highlighting the need for detailed long-term seabird monitoring, as well as building resilience into populations through policy measures that incorporate remedial action on major seabird conservation priorities. Research should focus on understanding how seabird foraging, in terms of functional responses and searching behaviour, is influenced by both changing discards and natural fish prey availability, and how they impact upon fitness. It is also essential to link individual-level responses with population-, community- and ecosystem-level change. Understanding these links is fundamental to ongoing seabird management and conservation, and an ecosystem-based approach to fisheries management.

Introduction

Commercial capture fisheries, especially trawling, discard huge quantities of unwanted fish and offal – it has been estimated that 8% of all fish caught worldwide is discarded, equating to >7 million tonnes of waste entering the marine environment each year (average between 1992 and 2001; Kelleher 2005). Given global demand for protein and severe threats to some fish stocks, this practice is not sustainable. Moreover, not only does discarding have direct negative impacts on target and nontarget stocks, it can also have deleterious ecosystem-level effects (Goñi 1998; Furness 2003; Diamond & Beukers-Stewart 2011). In particular, discards represent a superabundant food resource for marine scavengers such as seabirds, marine mammals and some fish and, consequently, have fundamentally altered marine food webs worldwide (Camphuysen et al. 1995; Oro 1999; Reeves & Furness 2002). Eliminating discards is necessary to ensure that fisheries are economically and environmentally sustainable. However, a ban on discards may have unforeseen knock-on consequences for the large scavenger community they support.

European Union (EU) countries manage their fisheries collectively through the EU Common Fisheries Policy (CFP), which governs EU fishing activity, as well as markets in fishing products and aquaculture. Despite significant amendments to the CFP in 2002, it has been widely criticized for its failure to deliver sustainable fisheries, its primary rationale. In an effort to address these failures and restore European fisheries to a sustainable level, in 2011 the European Commission proposed major changes to the CFP under 10-yearly review (a legal obligation) of the policy. With the adoption of an ecosystem approach to management, as defined in the European Marine Strategy Framework Directive (European Commission 2008), the core objectives of this reform are fivefold: a ban on discarding, managing stocks according to a maximum sustainable yield, increased regionalization, transferable fishing concessions and social sustainability (http://ec.europa.eu/fisheries/reform/index_en.htm). Disagreement between member states on the terms and time-scales of the changes has, at the time of writing, generated many Council amendments (Council of the European Union 2012), as well as other amendments proposed by the European Parliament. The time-scale for a ban on discards, which in practice means the retention on-board a vessel of would-be discardable fish for subsequent landing, continues to be hotly debated. The current General Approach agreed by the Agriculture and Fisheries Council is for a phased ban commencing with pelagic and industrial fisheries at the latest from January 2014 and leading to an eventual ban on discarding in all fisheries not later than 2019. The reform text on this issue is still unratified and timelines remain in square brackets (meaning the text is not confirmed), creating much uncertainty as to where and when discards will be removed from EU marine ecosystems. However, when a reduction is enforced, this will be a major environmental change for marine scavengers, such as seabirds, which exploit this abundant food resource.

Understanding all impacts of CFP reforms is of key importance, but we focus on the response of seabirds to discarding for a number of reasons. Firstly, the impact of discarding on the marine environment has received relatively little attention, but is a global problem that urgently requires research. Secondly, although many marine predators have learnt to exploit discards, seabirds are among the most conspicuous scavengers with a long history of association with fisheries worldwide (e.g. Hudson & Furness 1989; Arcos & Oro 2002; Garthe & Scherp 2003; Votier et al. 2004c, 2008a; Grémillet et al. 2008; Torres et al. 2011). This abundant resource has shaped seabird foraging behaviour (Bartumeus et al. 2010; Votier et al. 2010, 2013), breeding biology (Oro, Jover & Ruiz 1996), population dynamics (Oro et al. 2004) and community ecology (Wagner & Boersma 2011), indicating the seabirds might be significantly impacted by discard reforms. Moreover, circumstantial evidence suggests that in areas of high discarding rates, populations of scavenging seabirds have become artificially inflated (Furness 2003; Wagner & Boersma 2011). In spite of the benefits this abundant food source may provide, many scavenging seabirds continue to be more threatened than comparable bird groups, which is a consequence of the combined negative impacts of commercial fisheries (e.g. direct resource competition and bycatch mortality) and other human-induced threats (e.g. introduced predators in colonies, habitat degradation and pollution), which makes them a conservation priority (Croxall et al. 2012). Therefore, we discuss the impact of discard reforms on seabird populations in light of the wider policy implications of restoring and maintaining the resilience of seabird populations through site-based and ‘global’ interventions.

Although a reduction in discarding is generally welcomed in terms of marine ecosystem management and health (although there are alternative views; Zhou 2008), effective conservation requires horizon scanning to identify and potentially mitigate any negative impacts of change (Sutherland et al. 2008). In this review, we focus on the impact of discard reforms for seabird populations in the EU, but also consider the global-scale impact of discard declines. We highlight the potential for negative impacts, as well as positive opportunities presented by CFP reform in regard to the progressive ‘discard ban’. Moreover, we discuss ways in which the biggest change to fisheries management in a generation may integrate with current management of seabird populations, and briefly consider how lessons learnt in the EU may apply at a global scale.

Interspecific differences in discard consumption

Within the European Union, a large number of seabird taxa have been recorded following fishing vessels and feeding on discards (Table 1). However, these are dominated by a small number of mainly large generalist omnivores able to consume a wide range of different sized prey, which are also effective during interference competition. Many of these regular discard consumers are endemic to Europe or occur at globally significant levels (Table 1a). There is no evidence for any species being obligate scavengers; however, in certain populations some individuals feed almost exclusively on discards (Votier et al. 2004a,b), although there is much inter- and intrapopulation variation (Votier et al. 2008a). There are many other species that follow fishing vessels (Table 1b), but these (often smaller) taxa do so infrequently and are not known to consume significant quantities of discards. Further work is required to fully understand the significance of discards for this guild of small scavengers, but in general, the direct impacts of discard reforms will probably be limited to a relatively small number of large taxa and these restricted range species may be of conservation concern.

Table 1. Discard use by seabirds in the EU. (a) Seabird taxa known to regularly follow fishing vessels and extensively consume fishery discards. Also included are minimum estimated European or EU population sizes along with proportion of the global estimate. (b) EU breeding seabirds and migrants whose levels of discard use are undetermined, but are known to attend fishing vessels to scavenge
(a) Seabirds extensively exploiting fishery discards a
Breeding taxaEuropean population (breeding pairs)/% of global population (minimum estimates)
NE Atlantic
Black-legged kittiwake Rissa tridactyla2 410 673 / 48b
Herring gull Larus argentatus705 000 / 64b
Lesser black-backed gull Larus fuscus264 975 / 99b
Great black-backed gull Larus marinus100 000 / 58b
Great skua Stercorarius skua15 990 / 99b
Northern gannet Morus bassanus309 559 / 79b
Northern fulmar Fulmarus glacialis2 326 208 / 43b
Mediterranean
Audouin's gull Larus audouinii13 246 / 96c
Yellow-legged gull Larus michahellis340 910 / 90c
Balearic shearwater Puffinus mauretanicus9000 / 100c
Cory's shearwater Calonectris diomedea diomedea138 500 / 100c
Common tern Sterna hirundo220 000 / 48b
Sandwich tern Sterna sandvicensis69 000 / 43b
(b) Seabirds attending fishing vessels – infrequently using fishery discardsd
Breeding taxaMigrant taxa visiting EU waters
  1. a

    From the peer-reviewed literature (see text for references).

  2. b

    European populations and % estimate from Mitchell et al. (2004).

  3. c

    EU populations and % estimate from Snow & Perrins (1998).

  4. d

    From the peer-reviewed and grey literature (see text for references).

Black-headed gull Chroicocephalus ridibundusCaspian gull Larus cachinnans
Common gull Larus canusGlaucous gull Larus hyperboreus
Great black-backed gull Larus marinusSabine's gull Xema sabini
Little gull Larus minutusGreat shearwater Puffinus gravis
Slender-billed gull Chroicocephalus geneiSooty shearwater Puffinus griseus
Black tern Chlidonias nigerPomarine skua Stercorarius pomarinus
Leach's storm-petrel Oceanodroma leucorhoaLittle auk Alle alle
European storm-petrel Hydrobates pelagicusWhite-winged tern Chlidonias leucopterus
Little shearwater Puffinus assimilis 
Manx shearwater Puffinus puffinus 
Yelkouan shearwater Puffinus yelkouan 
Arctic skua Stercorarius parasiticus 
Common guillemot Uria aalge 
Great cormorant Phalacrocorax carbo 
European shag Phalacrocorax aristotelis 
Mediterranean shag Phalacrocorax aristotelis desmarestii 

Potential negative impacts of discard reform for seabirds

A significant reduction in or complete removal of discards is likely to impact seabirds directly by reducing food availability and altering at-sea distribution or indirectly via prey switching in the face of food shortage (Fig. 1).

Figure 1.

Potential effects of discard reform on seabird communities. Red boxes and arrows = negative consequence/impact, green boxes and arrows = positive consequence/impact, and dashed red line/arrows = possible effect dependent on natural fish stocks and severity of linked consequence. Yellow dotted line = encircles the factors that may vary regionally, and brown dotted line = encircles the factors that may be influenced by the wider impact of the Common Fisheries Policy reform.

Food shortage

For seabirds that feed extensively on discards, a reduction in or cessation of discarding could, in the absence of alternative food, create a major nutritional shortfall. The severity of this deficit will depend upon intra- and interspecific variation in discard consumption, as well as the potential for prey switching at the individual and population level. Here, we group species into foraging guilds based upon their prey range (niche width) at a population level, but also acknowledge that some generalist populations consist of many individual specialists.

Generalist omnivores

Large gulls and skuas are dietary generalists at the population level (consuming marine and terrestrial food), and many feed on discards. In the Mediterranean, gulls feed extensively on discards (up to 70% by biomass in their diet), particularly yellow-legged gull Larus michahellis (Naumann) and Audouin's gull L. audouinii (Payraudeau) (Oro et al. 1997; Arcos, Oro & Sol 2001; González-Solís 2003). Elsewhere in the EU, herring gulls L. argentatus (Pontoppidan), lesser black-backed gulls L. fuscus (Linnaeus) and great black-backed gulls L. marinus (L.) are also significant discard consumers (Garthe & Scherp 2003; Schwemmer & Garthe 2005). Discarding has profoundly altered many aspects of gull biology including foraging behaviour (Cama et al. 2012), demographics (Oro et al. 2004) and over-winter condition (Hüppop & Wurm 2000). Discard declines could influence foraging success, breeding performance, body condition and probably survival (of immatures, subadults and adults; see Oro et al. 2008) with the potential for population-level consequences. This is of concern given recent steep declines in some European large gull populations (Mitchell et al. 2004). Gulls may, however, be able to ameliorate any deleterious impacts by switching to alternative prey (Nocera & Kress 1996) (which may itself create problems, see 'Impacts of prey switching' below). Moreover, gulls are also known to respond to discard declines by moving into novel habitats such as inland and urban environments (Oro et al. 1997; Camphuysen, Camphuijsen & van Spanje 2006; Camphuysen et al. 2010).

Great skuas (hereafter ‘skua’) Stercorarius skua (Brunnich) are dominant scavengers at fishing vessels in much of their core breeding areas in northern and western Scotland (Mitchell et al. 2004) and also follow fishing boats during the nonbreeding season (Camphuysen & van der Meer 2005). Spatiotemporal changes in the consumption of discarded whitefish by skuas can be attributed to changes in fishing activity (Votier et al. 2004c, 2008a), indicating that despite appearing superabundant, fishery waste is limited. Skuas may therefore respond in a similar way to large gulls in the face of declining discards (i.e. in terms of breeding success), although there are currently no known links between discarding and skua reproductive biology. Skuas feed on a wide variety of nondiscard prey including sandeels Ammodytes sp, seabirds, mammals and goose barnacles Lepas lepas (Lamarck) (Votier et al. 2004a,b) and are able to switch to these alternative foods as discards decline, with potentially deleterious impacts on smaller seabirds via direct predation and competition for food (Votier et al. 2004a,b). However, in contrast to gulls, skuas are not known to undergo short-term range shifts into novel inland or urban environments.

Generalist piscivores

Northern gannets (hereafter ‘gannet’) Morus bassanus (L.), northern fulmars (hereafter ‘fulmar’) Fulmarus glacialis (L.), Balearic Puffinus mauretanicus (Lowe) and Cory's shearwaters Calonectris diomedea diomedea (Scopoli) all feed on a wide range of different fish, including discards. This broad niche width may enable these species to switch to feed on a range of fish prey in the face of discard declines.

Fulmars feed on a wide variety of prey, and offal is more important than whole fish discards (Ojowski et al. 2001). Offal will probably still be produced by fisheries irrespective of any downturn in discarding (e.g. Reeves & Furness 2002), meaning that this species may be less impacted by discard reforms. Furthermore, hydrographic features and the location of forage fish better predict the at-sea distribution of fulmars compared with the location of fishing vessels (Camphuysen & Garthe 1997; Skov & Durinck 2001).

Gannets do not feed on offal, but prefer discarded roundfish (Garthe, Camphuysen & Furness 1996). There is evidence of great dietary flexibility both among (e.g. Hamer et al. 2000; Garthe, Montevecchi & Davoren 2011) and within (Votier et al. 2010; Stauss et al. 2012) gannet populations, suggesting that they might be able to switch to feed on alternative prey such as pelagic fish in the face of a discard ban (Votier et al. 2013). Despite this, a key question is whether there are sufficient pelagic fish to meet the needs of gannets in the absence of discarding, particularly during the nonbreeding period when discards appear to be more important (Garthe, Camphuysen & Furness 1996; Camphuysen & van der Meer 2005).

Balearic shearwaters may be able to use a range of different fish in the face of a discard ban – stable isotope data indicate that they switch from pelagic fish to discards between incubation and chick-rearing (Navarro et al. 2009). However, interannual variability in breeding performance has been related to the availability of both small pelagic fish and trawler discards (Louzao et al. 2006), indicating that this critically endangered species may be negatively impacted by a discard ban.

Cory's shearwaters also make extensive use of discards, at least during the breeding season in the Mediterranean (Oro & Ruiz 1997; Martínez-Abraín, Maestre & Oro 2002). In the absence of discards, shearwater foraging becomes super-diffusive and spatially spread, probably affecting feeding rates and eventually breeding success (Bartumeus et al. 2010).

Specialist piscivores

For seabirds that specialize on small shoaling fish, the direct effects of a discard ban will be dependent on the condition of their natural prey stocks, partly a product of the strategy and management of pelagic fisheries. Sandwich Sterna sandvicensis (Latham) and Common terns S. hirundo (L.) extensively exploit discards in the Mediterranean (Oro 1999), probably benefiting from the predictability of this resource (Bartumeus et al. 2010). Discards are particularly important as compensatory food for these seabirds when their natural clupeid prey stocks (e.g. sardine Sardina pilchardus (Walbaum) and anchovy Engraulis encrasicolus (L.)) are scarce or overexploited. Strong regional and species-specific variation in the stocks of shoaling pelagic fish (Palomera et al. 2007) means the potential effects on specialist piscivorous seabird populations in the Mediterranean are uncertain. In the face of climate- and fisheries-mediated declines in sandeel Ammodytidae spp. availability in the NE Atlantic (e.g. Frederiksen et al. 2004), a similar imbalance between energy requirements and prey availability may influence other specialist seabirds that occasionally follow fishing vessels (e.g. kittiwakes, auks, small shearwaters).

Infrequent discard consumers

Many other seabird species (at least 17 EU breeders and 8 migrants) scavenge infrequently or opportunistically around fishing vessels during the breeding season (Oro & Ruiz 1997; Martínez-Abraín, Maestre & Oro 2002; Garthe & Scherp 2003; Valeiras 2003; Carboneras 2009; Louzao et al. 2011; Table 1). In many instances, the amount of food obtained via scavenging is not known, nor is the reproductive status of the birds following vessels, which together hamper our ability to determine the likely consequences of a discard ban.

Impacts of prey switching

Skuas and gulls are predicted to respond to discard declines by switching to feed on alternative prey (Oro, Bosch & Ruiz 1995; Oro, Jover & Ruiz 1996; Regehr & Montevecchi 1997), or increasing kleptoparasitism (Oro, Jover & Ruiz 1996; Martínez-Abraín et al. 2003), representing a threat to some seabird communities (Furness 2003; Votier et al. 2004b,c, 2006, 2007, 2008a). Predation rates can be very high; for example, a recent estimate of seabird consumption by great skuas at St Kilda, Scotland estimates that >47,000 seabirds are consumed per year (Miles 2010). Nevertheless, we have an incomplete understanding of prey switching among skuas and gulls. For instance, generalist populations are typically comprised of individual specialists (Votier et al. 2004a,b; Sanz-Aguilar et al. 2009), whose foraging behaviours are retained within and among seasons (Votier et al. 2004a) and may take several years to learn. Therefore, for those individuals that feed almost exclusively on discards, it is uncertain how effectively they may switch away from a scavenging lifestyle. Moreover, the impacts of predation may be ameliorated by density-dependent competition among predators (Votier et al. 2007) and/or by seabirds moving to breeding sites where predation risk is low (Votier, Heubeck & Furness 2008b).

Changes in at-sea distribution

Fisheries can strongly shape the at-sea behaviour and distribution of seabirds by providing a spatially and temporally predictable food source (Bartumeus et al. 2010; Cama et al. 2012) or by depleting prey stocks (Bertrand et al. 2012). Changes in discard availability may lead to increased foraging effort during breeding, or may alter over-winter distribution (Arcos & Oro 1996; Mañosa, Oro & Ruiz 2004; Kubetzki et al. 2009). An increase in time and energy expended while searching for natural, more unpredictable, food sources could incur a significant cost (Weimerskirch 2007). Although as yet untested, some seabirds may have learnt to find food by relying exclusively on fishing vessels as important visual cues. Moreover, the large aggregations of birds following fishing vessels may be more effective in terms of local enhancement (indication of potential food resources) than smaller aggregations of birds targeting natural prey (Votier et al. 2013).

Potential positive impacts of discard reform for seabirds

Reduced risk of bycatch

In the vast majority of cases, seabirds are attracted to fishing vessels for food. By reducing or removing discards, fewer seabirds will be attracted to vessels, reducing the risk of accidental bycatch. The attraction of seabirds to baited hooks in longline fisheries has long been known to be a major cause of seabird mortality – global estimates of >160,000 killed each year (Anderson et al. 2011). More recently, it has become clear that entanglement and collision with gear in trawl fisheries is also a major source of seabird mortality (Sullivan, Reid & Bugoni 2006; González-Zevallos, Yorio & Caille 2007; Favero et al. 2011). Reducing attraction to trawlers (by onboard retention of discards and offal) will help lessen mortality risk, and this is one of the mitigation measures recommended by the Food and Agriculture Organization of the United Nations (FAO) Best Practice Technical Guidelines for reducing bycatch (FAO 2008). However, a reduction in discard rates during a trawling moratorium in the Mediterranean led to higher attendance at longline fishing vessels, therefore increasing mortality risk (Laneri et al. 2010). This can only be resolved if all fisheries within a given region – whether trawl or longline – effectively implement fisheries practices needed to minimize incidental bycatch of seabirds.

Reduction in artificially high scavenger communities

Circumstantial evidence indicates that populations of scavengers, particularly large generalist predators, have become artificially inflated in areas of high discarding (see Furness, Ensor & Hudson 1992; Garthe et al. 1999; Oro & Martínez-Abraín 2007). These large despotic species dominate competitive interactions and can negatively affect the breeding performance of small neighbouring species (Oro et al. 2009). However, populations of generalist scavengers may decline following a discard ban easing negative top-down effects and changing the dynamics and regulatory pressures in seabird communities (Almaraz & Oro 2011). If this were to occur, this change in seabird community structure may represent a more ‘natural’ and sustainable state.

Knowledge gaps

Despite the wealth of research linking seabirds with discarding, there remain a number of key areas that are very poorly understood (Fig. 1).

Nonbreeding season

Many EU seabirds associate with fisheries during the nonbreeding period (e.g. Table 1; Arcos, Oro & Sol 2001; Cama et al. 2011). For example, in the North Sea during the 1990s it was estimated that outside the breeding season, discards were capable of supporting between 1·4 and 3·4 million scavenging seabirds (Garthe, Camphuysen & Furness 1996), and in the Canary Upwelling region, large numbers of nonbreeding seabirds co-occur with one of the largest fishing fleets in the world (Camphuysen & van der Meer 2005). Moreover, large numbers of migrant seabirds [e.g. sooty Puffinus griseus (Gmelin) and great shearwaters P. gravis (O'Reilly)] visiting EU waters are also regularly recorded following fishing vessels for food. Therefore, although it is clear that discards are important for seabirds during the nonbreeding season, few studies have accurately quantified the importance of scavenging at this time of the annual cycle (but see Grémillet et al. 2008). Nevertheless, there is evidence that discard availability can influence winter body condition in some seabirds (Hüppop & Wurm 2000) and that a low-quality diet during nonbreeding periods can carry over to have negative effects on reproductive success (Sorensen et al. 2009). The use of discards during the nonbreeding period may also be influenced by natural prey availability, which will regionally vary. For example, sandeels are not available during winter in the North Sea, which may increase the importance of discards for some wintering species. Conversely, small shoaling fish are available year round in the Mediterranean, possibly reducing the relative importance of discards. Future work should aim to plug this major knowledge gap in terms of nonbreeding season discard use, direct effects of this strategy, as well as potential carry-over effects.

Immature seabirds

Seabird populations typically contain large numbers of sexually immature individuals that rarely visit breeding colonies and these birds' cryptic lifestyles mean they are poorly studied (Votier et al. 2011). During this long period of immaturity, learning to effectively find food may be a key constraint (Dobson & Jouventin 2007) and therefore access to large quantities of easily accessible discards may influence survival to recruitment. Immature seabirds are regularly recorded behind trawlers, yet the extent to which immature seabirds scavenge has not yet been quantified (but see Grémillet et al. 2008; Votier et al. 2008a). The highly competitive feeding conditions at fishing vessels may limit discard availability for immature birds (Hudson & Furness 1989), but this has yet to be tested.

Junk food

The ‘junk food’ hypothesis attributes declines in the productivity of piscivorous marine vertebrates to a diet of low nutritional quality (Alverson 1992; Wanless et al. 2005; Österblom et al. 2008). A significant proportion of fisheries discards are demersal whitefish (e.g. cod Gadus morhua (L.), haddock Melanogrammus agelfinus (L.) and whiting Merlangius merlangus (L.)) that tend to have a low lipid content compared with pelagic fish that are ‘natural’ prey for seabirds (e.g. mackerel Scomber scombrus (L.), herring Clupea harengus (L.) and sandeels Ammodytes spp.), as well as high levels of some contaminants (Arcos et al. 2002). For this reason, discards may be considered junk food (Grémillet et al. 2008). This represents something of a paradox; evidence suggests that discarding has led to increases in some seabird populations (see; Camphuysen et al. 1995; Reeves & Furness 2002; Thompson 2006; Almaraz & Oro 2011), yet discards may be suboptimal as life-history parameters are lower when some seabirds feed on low-calorie prey (Litzow et al. 2002; Romano, Piatt & Roby 2006; Grémillet et al. 2008; Mullers et al. 2009). These incongruent theories may, in part, be explained by differences in digestive efficiency among species (Hilton, Furness & Houston 2000). Further research is required to understand how a discard diet may impact energetics of adult and young generalist seabirds with long gut retention times compared with species that feed primarily on lipid-rich fish that have short gut retention.

Ecosystem and community interactions

A change in fisheries management to promote sustainability (e.g. via a discard ban or increased gear selectivity) has the potential to increase the abundance of forage fish for marine predators and alter their abundance and distribution. An increase in other higher trophic-level predators, such as marine mammals and large fish, could alter ecosystem dynamics, for example, increasing top-down forcing at lower trophic levels, which may directly or indirectly affect prey availability for seabirds. Little is known about such multitrophic interactions and further work is needed to understand ecosystem-level responses. A first step is to combine ecosystem data in multitrophic-level models to better understand the impacts of change, but currently such studies are scarce (Lauria et al. 2012).

Wider implications of CFP reform for seabird conservation policy

Regionalization of fisheries management is a major component of the proposed CFP reform. This represents a move away from micromanagement at the EU level, but also to ensure that generic rules are tailored to suit fisheries at regional scales. This will inevitably lead to regional variation in fishing effort and/or discard availability, with relevance for seabird management.

Despite uncertainty about the impact of discard reforms on seabirds, the likely changes align quite well with current seabird conservation strategies. Croxall et al. (2012) recently identified a number of priority actions needed to help conserve seabird populations, and two should arise as a function of CFP reforms: a reduction in seabird bycatch and ensuring sustainability of fish stocks. However, the uncertainty and potentially negative impact of a discard ban means this issue should be added to the list of ongoing threats to seabird conservation. The increasing vulnerability of seabirds makes it all the more important to help build resilience into populations via firm remedial action on the major conservation priorities, notably habitat protection through site-based measures such as marine protected areas (MPAs) (Croxall et al. 2012). The potential changes in spatial distribution of fisheries as a consequence of reforms to the CFP (e.g. via restricted access to areas and real-time closures) may also influence the protection of at-sea resting and feeding areas, although this area of research is currently under-represented.

Discards are declining worldwide, and therefore current impacts on seabirds in the EU may be relevant at a global scale. Guilds of large generalist predators dominate scavenger communities in temperate and high-latitude waters throughout the world, and these species are likely to respond in similar ways to European seabirds (e.g. Regehr & Montevecchi 1997). Far less is known about discard use and seabird fishery interactions in tropical waters, although the limited evidence indicates that tropical seabird scavengers are dominated by smaller species such as terns Sterna spp. (Blaber et al. 1995).

Conclusions and recommendations

It seems unlikely that if discarding were to decrease or stop altogether, this would represent a crisis for most seabird populations in the EU. In the past few decades, global discards have been declining (Oro 1999; Kelleher 2005; Zeller & Pauly 2005), and although many seabird populations have shown significant downward trends during this period (Croxall et al. 2012), this does not appear attributable to declining discards.

The very opportunistic nature of scavenging species suggests that they may be able to adjust well to change, but for species that prey on other seabirds there is potential cause for concern. In this instance, monitoring of predation rates is essential to fully evaluate this impact. Conversely, reducing discards may actually have positive effects by decreasing rates of seabird bycatch, although it is unlikely to reduce long-line entanglement. Therefore, discard reforms have relevance for the EU Action Plan for reducing incidental catches of seabirds in fishing gears http://ec.europa.eu/fisheries/cfp/fishing_rules/seabirds/seabirds_communication_en.pdf. Nevertheless, a discard ban represents a potential new short- to medium-term pressure on scavenging seabirds and underlines the need for building resilience into seabird populations through other CFP reforms and policy measures designed to mitigate the diverse marine impacts on them.

Our review highlights the likelihood of strong regional-level responses to reduced discards and that certain species and communities will be impacted more than others. Applied research and monitoring should be directed towards species known to be heavily reliant on discards (Table 1a) and in EU regions where seabird communities contain many scavengers (e.g. West Scotland, North Sea, Mediterranean). Furthermore, diagnosing potential impacts of changing discards requires long-term studies. This is to provide sufficient statistical power to control for other potentially confounding environmental drivers of change, and because the low reproductive rates and high survivorship of seabirds mean that changes in demography may take many years to manifest themselves. Studying prey choice and foraging behaviour throughout the annual cycle and across age classes is also important because these may be sensitive to short-term changes in discarding. Furthermore, a key goal is to determine the shape of the multispecies functional response of scavenging seabirds, because this will determine how scavengers respond to change and the impact of predation on prey populations. Managing seabird populations is daunting because of the spatial scale at which they live. However, effective protection of breeding, feeding, resting and flyways, along with provision of sufficient food in the absence of discards, would certainly go some way to ensuring sustainability. This relies on substantial financial investment, but has the potential to provide an indication of overall marine ecosystem health and thereby help support obligations under international biodiversity conventions (Parsons et al. 2008; Durant et al. 2009). To make EU fisheries economically and environmentally sustainable in the context of an ecosystem-based approach, the politicians and policy makers need to agree and implement important reforms to the CFP, including the ban on discards. If enforced, it can enable a transition to sustainable fisheries with low impact on local ecosystems and biodiversity.

Acknowledgements

This work was funded by the Royal Society for the Protection of Birds and a Natural Environment Research Grant (NE/H007466/1). Thanks to Euan Dunn and Kara Brydson, and two anonymous reviewers, for commenting on this manuscript.

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