Bivalve ¢Shing and Maerl-Bed Conservation in France and the UK}Retrospect and Prospect

Home , Dosinia exoleta, Dragonet, Maerl

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS Aquatic Conserv: Mar. Freshw. Ecosyst. 13: S33–S41 (2003) Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/aqc.566

Bivalve ¢shing and maerl-bed conservation in France and the UK}retrospect and prospect

J.M. HALL-SPENCERa,*, J. GRALLb, P.G. MOOREc and R.J.A. ATKINSONc a School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK b Institut Universitaire Europeeen! de la Mer, LEMAR UMR-CNRS 6539, Place Copernic, Plouzane, France c University Marine Biological Station, Millport, Isle of Cumbrae, KA28 0EG, UK

ABSTRACT 1. Maerl beds are carbonate sediments, built by a surface layer of slow-growing coralline algae, forming structurally fragile habitats. 2. They are of international conservation significance, often supporting a high biodiversity and abundant bivalve molluscs. 3. Experimental fishing for scallops (Pecten maximus) on French and UK grounds has shown that although large epifauna are often killed, many organisms escape harm as they burrow deeply or are small enough to pass through the dredges. 4. Bivalve dredging is currently one of the main threats to European maerl grounds as it reduces their biodiversity and structural complexity and can lead to long-term degradation of the habitat. 5. Protecting maerl grounds is of importance for fisheries since they provide structurally complex feeding areas for juvenile fish (e.g. Atlantic cod - Gadus morhua) and reserves of commercial brood stock (e.g. Ensis spp., P. maximus and Venus verrucosa). 6. We outline improved mechanisms to conserve these ancient and unique biogenic habitats. Copyright # 2003 John Wiley & Sons, Ltd.

KEY WORDS: maerl; biodiversity; conservation; scallop dredging; bivalves; Scotland; France

INTRODUCTION

Maerl beds are sedimentary deposits derived from calcareous red seaweeds (Rhodophyta) that occur in coastal areas worldwide (Bosence, 1983; Littler et al., 1991; Steller and Foster, 1995) but are being degraded by a number of human activities (BIOMAERL, 1999). Their distribution is patchy and restricted by their need for light coupled with an intolerance of desiccation and low salinities (Birkett et al., 1998). Live maerl is limited to depths 532 m in the relatively turbid inshore waters of northern Europe. Maerl growth requires a degree of shelter from wave action, to prevent burial and dispersal into deep water, and enough water movement to prevent smothering with silt (Hall-Spencer, 1998). The special status of maerl grounds

*Correspondence to: Dr J.M. Hall-Spencer, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK.

Copyright # 2003 John Wiley & Sons, Ltd. Received 4 April 2001 Accepted 20 August 2002 S34 J.M. HALL-SPENCER ET AL. derives from their unique character as complex biogenic structures of great antiquity (Adey and McKibbin, 1970; Canals and Ballasteros, 1997; Hall-Spencer, 2001). The complex architecture and extreme longevity of these habitats accounts for their high biodiversity (Maggs, 1983; Grall and Gleemarec,! 1997; Birkett et al., 1998; Hall-Spencer, 1998; BIOMAERL, 1999). In Europe, there are moves to establish Marine Protection Areas (MPAs) following agreements such as the Rio de Janeiro Convention on Biodiversity (1992) and the EC ‘Habitats Directive’ (1992). Notably, the maerl-forming corallines Phymatolithon calcareum and Lithothamnion corallioides are currently the only two algae specified as requiring management under the EC ‘Habitats Directive’ (Annex V). Biogenic reefs, such as maerl beds, are accepted as being vulnerable habitats by France and the UK and have been included within a proposed network of conservation areas termed ‘Natura 2000’ sites (Holt et al., 1998; French Government Website, 2001). Over the past six years, EC-funded research has provided a rounded insight into the ecological conditions, population dynamics and significance of a variety of human impacts on European maerl beds (BIOMAERL, 1999). It is now clear that bivalve dredging is one of the major threats to these habitats. In this paper we outline key findings from our work on maerl beds in the Bay of Brest (NW France) and the Clyde Sea area (SW Scotland) to assess the past and future impacts of bivalve fishing.

THE TOPIC AS VIEWED FROM DIFFERENT PERSPECTIVES

Conservation of maerl habitats requires urgent attention since there is considerable potential for their accelerated and widespread degradation over the next decade (BIOMAERL, 1999). Here we present ‘devil’s advocate’ arguments that some might use in favour of current practices or in targeting a wider range of maerl-dwelling bivalves. We then highlight the negative aspects of unrestricted exploitation and call for the long-term protection of a range of maerl habitats.

ARGUMENTS IN FAVOUR OF BIVALVE EXPLOITATION ON MAERL BEDS

The main commercial target of NE Atlantic maerl beds is currently the scallop Pecten maximus. This species can exhibit good recruitment and growth on maerl beds due to low siltation and high rates of water exchange (Thouzeau and Lehay, 1988; Hily et al., 1992; Hall-Spencer and Moore, 2000a, c). Of 242 maerl beds recently surveyed around the UK, only about one third supported P. maximus (MNCR database, 2000). Where scallops do occur on maerl, strong currents and shallow plankton-laden water encourage the growth of large, high quality scallops that provide an attractive target for exploitation (Briggs, 2000). As northern European populations of maerl mainly reproduce through a cycle of fragmentation and growth (Cabioch, 1970; Freiwald et al., 1991), it has been argued that dredging can potentially benefit the spread of live maerl, allowing the colonization of new areas of sediment. However, experimental studies have shown that dredged maerl tends to become crushed and buried leading to high levels of mortality due to lack of light (Hall-Spencer and Moore, 2000a). When maerl grounds are first dredged, debris and non-target invertebrate species such as sponges and Limaria hians nests are gradually removed from the ground and this improves subsequent dredge efficiency (Hall-Spencer and Moore, 2000b). Although large, fragile epibenthos (e.g. the sea urchin Echinus esculentus) are killed, hard-shelled organisms (e.g. the whelk Buccinum undatum) often survive. Scallop dredges are designed to allow young scallops to pass through and many survive to be harvested in future years (Caddy, 2000). Provided there is a consistent supply of spat, dredged areas can yield substantial catches year on year. Schemes to improve spat supply are in place on maerl grounds in the Bay of Brest, which are re-seeded with hatchery-reared juveniles (Hall-Spencer et al., 2001).

(a) BRITTANY 80

40 mean no. taxa 20

0 BC AC BI AI AC AI AC AI AC AI Summer Autumn Winter Spring 0.1 m2 grab samples

(b) SCOTLAND 80

40 mean no. taxa 20

0 BC AC BI AI AC AI AC AI AC AI Summer Autumn Winter Spring 0.1 m2 grab samples Figure 1. Mean number of taxa from 1 mm-sieved 0.1 m2 grab samples in control (open columns) and test areas (shaded columns) before and after experimental scallop dredging on maerl in the Bay of Brest (Brittany) and the Clyde Sea (Scotland). X-axis codes starting with ‘B’ denote ‘before ﬁshing’, ‘A’ denotes ‘after ﬁshing’. ‘C’ denotes ‘control plot’ samples, ‘I’ denotes ‘impacted plot samples. Error bars are +S.D. (n ¼ 6).

Although current bivalve dredging practices do alter maerl habitats (Hall-Spencer and Moore, 2000a), they do not lead to long-term devastation of target species or the creation of barren grounds. Certain maerl grounds in the Bay of Brest have been dredged for scallops and the infaunal bivalve Venus verrucosa for >40 years, yet these sites remain productive for commercial bivalves and retain high levels of live maerl cover (Hall-Spencer et al., 2001). The sustained live maerl cover in the Bay of Brest may relate to local restrictions which set a limit of one scallop dredge per boat; this probably causes less damage than the sets of 36 dredges that are used routinely by large UK scallop boats. Typical French and UK scallop dredges have ca 10 cm long teeth to extract scallops living recessed within the sediment. The majority of inhabitants in the upper 10 cm of maerl sediment are small macrofauna. Grab sampling over the past two years showed that the number of taxa remained high after dredging maerl in the Bay of Brest and the Clyde Sea area (Figure 1). Small organisms survived in high numbers as many were displaced on a ‘bow wave’ that disturbed the sediment ahead of the advancing gear (see Gilkinson et al., 1998).

Copyright # 2003 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 13: S33–S41 (2003) S36 J.M. HALL-SPENCER ET AL.

Maerl communities have a degree of resilience to scallop dredging as many organisms often live below the depth raked through by the dredge teeth (Keegan and Koonnecker,. 1973; Hall-Spencer and Atkinson, 1999). Deep-burrowing organisms can represent the majority of infaunal maerl biomass and can survive dredging in high numbers (Hall-Spencer et al., 2001). This work has also revealed that maerl beds represent a huge, presently untapped, source of edible infaunal bivalves. The hydraulic technology needed to exploit these populations is available and supports an extensive fishery in Italian waters (Froglia, 1989). A rapidly developing UK fishery for razor clams (mainly Ensis siliqua) is proving profitable, based on hand-collection on sandy sediments. There are also global markets opening up for the export of other maerl-dwelling bivalves such as Dosinia exoleta, Tapes rhomboides and Venus verrucosa. If such resources could be exploited sustainably, this could bring much needed employment and benefits to rural communities.

ARGUMENTS AGAINST BIVALVE EXPLOITATION OF MAERL BEDS

Scallop dredging on French and UK maerl beds has significantly reduced the complexity, biodiversity and long-term viability of these habitats (Hily et al., 1992; MacDonald et al., 1996; Hall-Spencer and Moore, 2000a-c). A major reason for concern over the vulnerability of NE Atlantic maerl to damage from any source is its very slow rate of growth (Cabioch,1970; Potin et al., 1990), such that substantial deposits take centuries, or millennia, to accumulate (Freiwald et al., 1991; Birkett et al., 1998). Hall-Spencer and Moore (2000c) illustrated the substantial reduction in size between maerl thalli of Phymatolithon calcareum from museum collections made in 1891, cf. material collected from the same site in 1995, which they attributed to mechanical impacts of scallop dredging. When a pristine Clyde Sea maerl bed was damaged by experimental scallop-dredging, there was no measurable recovery, in terms of area of living maerl, over a period of five years. This bed was susceptible to burial since the maerl lay in a thin layer on the surface of muddy sand. The documented effects of hydraulic dredging for infaunal bivalves on other sediments (Anon., 1998) is strong evidence that this would also have detrimental long-term effects on maerl. Such damage should be avoided, particularly as European fisheries are set to benefit from the protection of maerl grounds as they provide ‘essential fish habitat’ (sensu Auster and Langton, 1999) and refugia for bivalve brood stocks. Maerl contrasts with most sediments (muds and sands) in that it forms structurally complex deposits of shells and interlocking thalli (Plate 1). Often there are gravel ripples (created by strong currents or waves) and cobble- and pebble-sized rocks that increase the heterogeneity of the habitat. Dead shells, rock crevices and maerl thalli act as shelters for small motile animals including polychaetes (Grall, pers. obs.), amphipods (Moore, 1984; De Grave, 1999), squat lobsters (Hall-Spencer et al., 1999), and gobies (Miller, 1986). The solid surfaces have gastropod grazers (Farrow and Clokie, 1979) feeding on attached algae including crustose species and kelps that reach several metres into the water column (Maggs, 1983). Faunal constructions add further to the secondary architecture of the ground and include soft-bodied colonial organisms (e.g. sponges and tunicates), annelid faecal mounds, thalassinidean crustacean mounds, pits left by scallops and feeding crabs together with substantial clumps of reef-builders (e.g. Modiolus modiolus, Limaria hians). Underneath this surface complexity are cerianthid anemone burrows, chaetopterid polychaete tubes and all kinds of tunnels. These structural complexities provide shelter and enhance the array of prey items available to fish. Dragonets (Callionymus lyra, Plate 1) and shoals of juvenile cod (Gadus morhua, Hall-Spencer and Moore, 2000b) feed over Scottish maerl grounds, for example. Habitat complexity and emergent biota significantly reduce 0-yr mortality in Atlantic cod (Gotceitas and Brown, 1993; Lindholm et al., 1999; modelled theoretically by Walters and Juanes, 1993) a species in urgent need of conservation measures, since overfishing has brought stocks near to economic extinction (Hutchings, 2000). Maintaining maerl habitat complexity would be likely to benefit juvenile commercial fish.

Copyright # 2003 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 13: S33–S41 (2003) Plate 1. Dragonet (Callionymus lyra) on maerl habitat in Loch Torridon, Scotland in February 2001. Note the structural complexity of the maerl mixed with shells and kelp holdfasts (Laminaria saccharina). Photograph by Scottish Natural Heritage.

40 Dosinia exoleta

20 frequency 10

0 1 5 6 10 11 15 16 20 21 25 26 30 31 35 36 40 41 45 46 50 51 55 56 length (mm)

Figure 2. Size-frequency distribution of Dosinia exoleta collected in thirty 0.5 m2 4 mm sieved suction samples from maerl at 10 m C.D. Loch Fyne, Scotland 1999-2000.

Maerl habitat complexity is much reduced by bivalve dredging. Physical irregularities are flattened, the maerl is compacted and disturbed silt settles over a wide area smothering algae, which require light for photosynthesis (Hall-Spencer and Moore, 2000c). Although small organisms, deep burrowers and heavily armoured species often survive, much of the large epibenthos is killed. Even deep-burrowing species will be vulnerable for critical periods when juveniles are present in the surface sediment. Many bivalve species recruit intermittently, sometimes with decades elapsing between successful spatfalls (Stephen, 1938; Ansell, 1972; Berthou, 1983; Beukema and Dekker, 1995). Damage to these species during recruitment could therefore have long-lasting consequences. The resilience of certain maerl fauna (i.e. small infauna and deep burrowers) should not lead to uncontrolled exploitation, as the best maerl beds represent ‘jewels in the crown’ of inshore biodiversity. Grounds that are extensively dredged have reduced population densities of surface megafauna (Hall-Spencer and Moore, 2000b, c) and a much lower diversity of colonial suspension feeders (De Grave and Whitaker, 1999a) and molluscs (Hall-Spencer, 1998). Recent quantitative information on the deep-burrowing fauna of European maerl beds has shown that infaunal bivalves can represent an extremely high biomass (>20 g ash-free dry weight per 0.5 m2) that is currently unexploited in the UK. Work at a site in the Clyde Sea area showed that the edible bivalve Dosinia exoleta was particularly common (ca 40 m2). Mature individuals measuring around 48–50 mm shell length were dominant in the population (Figure 2). Basic ecological information is lacking on the sustainability of deep-burrowing bivalve expoitation. However, if growth rates are similar to those recorded in SW Norway (Tunberg, 1983), these large D. exoleta will be more than 10 years old. We foresee environmental problems emerging if fishing for long-lived deep-burrowing bivalves (like D. exoleta, Ensis arcuatus, Venus verrucosa) becomes more widespread both by hand (scuba diving) or mechanically (hydraulic dredging). Since 1994, financial support through European Union PESCA and other initiatives has encouraged diversification of European fishing fleets such that there is real potential for harmful commercial exploitation of maerl infaunas. As economic and political pressures mount on fishers to shift into presently under- or unexploited stocks, there is an urgent need to protect pristine maerl beds since the consequences of even one minor experimental dredging episode can be wide-ranging and long-lasting (Hall- Spencer and Moore, 2000a-c). Maerl habitat conservation would help sustain shellfish fisheries as a whole, as these grounds provide brood-stock areas for bivalves (Hall-Spencer, 1998) and can greatly enhance recruitment of juvenile scallops (Thouzeau and Lehay, 1988; Steller et al., 2003). Since there is no collateral environmental damage caused by divers hand-collecting scallops (cf. dredging) it seems, at first sight, logical to favour this method of harvesting bivalves from shallow-water maerl grounds. Briggs (2000) noted, however, that a disadvantage with diver fisheries is that they tend to focus on large individuals from areas that are

Copyright # 2003 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 13: S33–S41 (2003) S38 J.M. HALL-SPENCER ET AL. generally inaccessible to dredges. It is likely that these, otherwise inaccessible, individuals make up an important component of the population brood stock that could be essential for sustained recruitment of juveniles to the wider ﬁshed stock. When Ensis spp. are collected by hand they are usually forced from their burrows by pouring salt onto their siphons. The large amounts of salt used poses an additional threat to the infauna of maerl habitats. Consequently, protection of relatively small areas represented by maerl-bed metapopulations of commercial bivalve species (cf. Wolff and Mendo, 2000) makes sound economic sense. Protection of restricted areas such as maerl beds would help ensure that mature, fecund bivalves provide spawn to re-seed wide areas where the marine habitats are less sensitive to the effects of bivalve dredging.

CONCLUSIONS

We have discussed the trade-offs concerning current and future ways in which French and UK maerl habitats are fished. Any short-term benefits must be weighed against the long-term costs of environmental damage, as must benefits to a few versus the costs to many. On balance, our research indicates that society has more to gain from protecting maerl habitats than it has from their destructive exploitation. The EC’s ‘Habitats Directive’ (1992) demands that exploitation of maerl habitats in European seas must be compatible with their maintenance at a ‘‘favourable conservation status’’ but this stricture is largely ignored (BIOMAERL, 1999). It is welcome that the need to conserve maerl habitats has influenced the choice of a network of Natura 2000 sites in European waters (Birkett et al., 1998). Though unpublished databases are expanding for the UK (White, 1999; MNCR, 2000) and France (Augris and Berthou, 1990), detailed reviews of the extent, distribution and status of European maerl beds are needed, similar to that recently published for Ireland (De Grave and Whitaker, 1999b). Good examples of maerl habitat are known to occur around France and the UK, but there is an immediate risk of rapid expansion in destructive practices, particularly with respect to the exploitation of long-lived infaunal bivalves. We would recommend that the opportunity is taken to introduce (and enforce) stringent restrictions on bivalve dredging to protect brood stock at the earliest possible opportunity. Maerl beds vary in terms of their physical (e.g. size and granulometric structure) and biological composition so are not all equally vulnerable to dredging. The burden of proof regarding exploitation should lie with those intending to utilize these habitats. We suggest a general presumption of protection, particularly if the following criteria apply: * Biogeographical significance of habitat. If maerl habitat is very rare in a particular country, as it is in England (Jones et al., 2000), then any maerl beds there should be protected. * Shallowness of surficial layer. Maerl beds with a shallow layer of live thalli or those that overlie silt/clay are particularly vulnerable to smothering or burial by towed fishing gear. * Percentage live maerl cover. Maerl grounds with 100% cover of living thalli are unusual and should be protected from damage. * Size of maerl thalli. Large maerl thalli (e.g. >4 cm) are fragile and would be readily broken up by contact with dredges (Hall-Spencer and Moore, 2000a). * The presence of rare species of maerl. Some maerl-forming species are very scarce (e.g. Lithophyllum dentatum in Ireland; Birkett et al., 1998) and need to be protected from damage. * The presence of vulnerable epifauna. Considerable losses of large and superficial species (e.g. Limaria hians, Modiolus modiolus, massive sponges) have taken place in heavily fished sites. Remaining strongholds for such species should be protected. * Pristine sites. Mankind has altered many maerl beds, so those with no history of impact should be protected from future degradation. The pressing need for unexploited sites, against which to judge anthropogenic effects, would justify their protection.

* Importance for commercial species. Maerl beds should be protected where they are important as brood stock areas for bivalves or form ‘essential fish habitat’ such as feeding areas for juvenile cod (Auster and Langton, 1999; Hall-Spencer and Moore, 2000b; Jones et al., 2000) As maerl beds are effectively non-renewable resources (BIOMAERL, 1999), we favour invoking the Precautionary Principle (Gray and Bewers, 1996), and advocate that a presumption of protection should be introduced for all maerl beds. There is now strong evidence that by conserving a network of maerl habitats, these relatively small areas would harbour bivalve brood stock (e.g. Ensis spp., Pecten maximus, Venus verrucosa) that would reseed adjacent fishing grounds. In addition, major proportions of inshore biodiversity would be protected within these localized areas of ancient biogenic habitat providing ‘essential fish habitat’ for commercial fish.

ACKNOWLEDGEMENTS

This work was partly funded by the European Commission (CFP Study Project 98/018) and a Royal Society Research Fellowship to JH-S. This study neither reﬂects the views of the European Commission nor its future policy in this area. We thank the crews of RV ‘Aora’ (UMBSM), RV ‘Cotes d’Aquitaine’ (CNRS INSU) and FV ‘Barakuda’ (Per LeGall and Jackez Kervella) together with the divers Ken Cameron, Hugh Brown, Garnet Hooper (UMBSM) and Laurent Chauvaud, Sylvain Chauvaud, Laurent Gueerin,! Freed! eeric! Jean, Maryvonne Le Hir, Robert Marc, Jean-Pierre Oldra, Coralie Rafﬁn and Geerard! Thouzeau (IUEM). Thanks also to the student helpers Benjamin Guyonnet, Guillemette Joly, Jeerome! Jourde, Fanny LeFur, Helen Rae, Alexandre Vagne and Emma Walker. Our collegues Jean Pierre Carval, Chris Houton, Yves-Marie Paulet, and Alphonse Tram were also supportive throughout.

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