Katie sambrook

1

Running head: Monitoring of maerl beds

2

Mapping and monitoring the maerl beds in the Fal & Helford Special Area of Conservation:

3

a review of techniques

4

Katie Sambrook*, Trudy Russell

5

Falmouth Marine School, Killigrew Street, Falmouth, Cornwall, TR11 3QS

6

Abstract

7

Maerl is a generic term for several species of unattached, non-geniculated coralline red

8

algae. Maerl beds are considered to be of conservation importance due to their rarity,

9

environmental sensitivities and high biodiversity and are subject to both UK and European

10

legislation. The EU Habitats Directive resulted in the creation of a network of Special Areas

11

of Conservation, established to provide a degree of governance for key habitats and species.

12

The Fal & Helford Special Area of Conservation contains the largest live maerl bed in

13

southwest Britain. Conservation targets for maintaining the favourable condition of these

14

maerl beds include monitoring the extent, distribution, percentage of live maerl and species

15

composition. It is a requirement that these attributes are assessed every six years. This

16

review evaluates existing techniques used for subtidal benthic habitat mapping and

17

biodiversity surveys recommending suitable methods for monitoring maerl in the Fal &

18

Helford Special Area of Conservation.

19

20

Keywords

21

Maerl, habitat mapping, special area of conservation, biodiversity, monitoring, surveys *Corresponding author. Email: katie.sambrook@hotmail.co.uk

1

22

23

Introduction

24

25

Maerl is the generic term for unattached, non-geniculated coralline red algae (Birkett et al.

26

1998, Foster 2001). It has a hard calcium carbonate skeleton which research indicates

27

makes a significant contribution to carbon sequestration in the oceans (Canals & Ballesteros

28

1997, Birkett et al. 1998). Maerl beds form when living and dead maerl thalli accumulate,

29

with accretion occurring over long periods due to the slow growth rate of maerl, usually

30

between 0.05 and 1.0mm y-1 (Birkett et al. 1998, Foster 2001, Bosence & Wilson 2003, Grall

31

& Hall-Spencer 2003). Found in polar, temperate and tropical waters, maerl-forming species

32

are patchily distributed due to narrow environmental tolerances (Barbera et al. 2003, Grall

33

& Hall-Spencer 2003).

34

distribution of maerl as it is intolerant to smothering and burial (Birkett et al. 1998, Barbera

35

et al. 2003). Light, temperature and salinity also contribute to its spatiotemporal presence

36

(Birkett et al. 1998, Barbera et al. 2003, Wilson et al. 2004, Sciberras et al. 2009). Three

37

species of maerl are found to contribute to the majority of maerl beds in the UK,

38

Lithothamnion corallioides, Lithothamnion glaciale and Phymatolithon calcareum, the latter

39

being predominant (Birkett et al. 1998).

Current flow is the primary abiotic factor that influences the

40 41

The nodular structure of maerl creates an interlocking matrix providing a habitat for a wide

42

range of infauna and epifauna (Birkett et al. 1998, Barbera et al. 2003). This lattice

43

formation is responsible for the high biodiversity found on maerl beds which is comparable

44

to other algal biotopes such as sea grass beds and kelp forests (Birkett et al. 1998, Kamenos 2

45

et al. 2004a). As well as exhibiting high biodiversity, maerl beds have been found to harbour

46

juveniles of commercially important species such as gadoids and the queen scallop

47

Aequipecten opercularis (Kamenos et al. 2004b, c, d). Studies in Scotland found that the

48

highest densities of juvenile cod (Gadus morhua), saithe (Pollachius virens) and pollack

49

(Pollachius pollachius) were observed between September and November (Kamenos et al.

50

2004b); and for A. opercularis between October and December (Kamenos et al. 2004b).

51

Although pristine live maerl beds (PLM) exhibit higher biodiversity, the long-term

52

accumulation of dead maerl deposits also represent an important habitat, particularly for

53

burrowing species (Birkett et al. 1998). Functional diversity on maerl beds is high with Grall

54

& Glémarec (1997) identifying eight trophic groups on a maerl bed in France.

55 56

Recognising the ecological importance of maerl, both L. corallioides and P. calcareum are

57

included in Annex V of the European Union’s Habitats Directive as species whose

58

exploitation is subject to management and are listed under the UK Biodiversity Action Plan

59

as priority species (Council Directive 92/43/EEC 1992). Maerl beds ares also protected under

60

Annex I of the Habitats Directive and appears on the Convention for the Protection of the

61

Marine Environment of the North-East Atlantic (OSPAR) list for threatened or declining

62

habitats and species. The Habitats Directive resulted in the creation of a number of Special

63

Areas of Conservation (SACs) established to provide a degree of governance and protection

64

to key habitats and species.

65 66

The Fal & Helford SAC is located in Cornwall and covers 6387.8 hectares (JNCC 2011). It

67

includes a range of Annex I habitats including ‘sandbanks which are slightly covered by

68

seawater all the time’ which contains the sub feature of maerl beds (JNCC 2011). The SAC 3

69

has the largest live maerl bed in southwest Britain, found on St Mawes Bank, and also

70

contains deep deposits of dead maerl gravel indicating that during the past live maerl was

71

much more prevalent than today (Birkett et al. 1998).

72 73

A number of studies have been conducted on the extent and biodiversity of maerl in the Fal

74

& Helford SAC. Blundel et al. (1981) recorded that live maerl was found at depths of 0-10m

75

in the Fal & Helford SAC; Davies & Sotheran (1995) mapped the extent of live and dead

76

maerl as part of the BioMar project; Perrins et al. (1995) compared the percentage of live

77

and dead maerl on St Mawes Bank between 1982 and 1992; Frau-Ruiz et al. (2007) surveyed

78

Falmouth Bay to establish the presence of maerl to inform decision-making on scallop

79

dredging and ship anchoring and Axelsson et al. (2008) undertook an ecological survey as

80

part of an appropriate assessment for the Port of Falmouth Development Initiative which is

81

currently seeking to dredge a part of the SAC in order to deepen the channel and increase

82

ship access.

83 84

The morphology and community structure of the maerl is likely to have changed since

85

Davies & Sotheran (1995) mapped the biotopes in the estuary. At this time both aggregate

86

dredging and scallop dredging were allowed within the site, although both activities were

87

banned in 2005, with the scallop dredging ban extending into Falmouth Bay in 2008 (Hall-

88

Spencer 2005, legislation.gov.uk 2008). Both practices are known to be destructive with

89

research into maerl beds in other regions showing that scallop dredging can lead to >70%

90

reduction in live maerl coverage with no indication of recovery during the subsequent four

91

years (Hall-Spencer & Moore 2000). Due to its slow growth rates and intolerance to

4

92

activities that create sediment perturbation and siltation, maerl is now recognised as a non-

93

renewable resource (Barbera et al. 2003).

94 95

In the UK to date, most surveys on maerl have been in relation to disturbance activities with

96

limited time-series data collected (OSPAR 2010). However, in order to maintain the integrity

97

of the SAC designation, it is fundamental that a monitoring programme is implemented to

98

conduct regular assessments of the protected habitats or species enabling early detection of

99

changes such as a decline in live maerl, issues with invasives, effects of climate change or

100

regime shifts (Birkett et al. 1998, Hiscock 1998, Sciberras et al. 2009). Conservation targets

101

under OSPAR and the Habitats Directive for maintaining the favourable condition of maerl

102

beds include monitoring the extent, distribution, percentage of live maerl, species

103

composition as well as recording the abiotic factors that could impact the health of the

104

maerl (OSPAR 2010). These checks are required at six-yearly intervals (Malthus & Karpouzli

105

2003, OSPAR 2010).

106 107

This paper seeks to evaluate current methodologies for obtaining this information, review

108

examples of good practice and make recommendations on the techniques that would work

109

best for the collection of data pertaining to the maerl in the Fal & Helford SAC. It does not

110

aim to provide detailed methodologies on how the surveys should be carried out. While

111

each site should be reviewed separately to assess potential threats specific to its location

112

and activity levels, it is a long-term aim that a standard protocol could be implemented

113

across other SACs containing maerl to establish a comprehensive network of data

114

contributing to its long-term sustainability.

115 5

116

Methods

117

118

Mapping the extent and distribution of maerl

119

The Fal & Helford SAC contains a busy port, has many recreational users and is home to the

120

only oyster fishery worldwide still fished under sail using traditional methods of dredging

121

(Challinor et al. 2009). An understanding of the extent and distribution of the live and dead

122

maerl is essential for informing decision-making surrounding the management and

123

conservation of this site.

124

125

Remote sensing

126

Recent technological advances have seen the development of remote sensing techniques

127

such as airborne sensing (aerial photography or video and hyperspectral data), satellite

128

imagery and acoustic sensing to support biotope mapping (Held et al. 2003, Diaz et al. 2004,

129

Godet et al. 2009). The use of remote sensing in the marine environment is advantageous

130

over traditional approaches such as grab sampling or dredging as it allows large areas to be

131

mapped over short timescales (Brown et al. 2002, Sciberras et al. 2009, Simons & Snellen

132

2009; Brown et al. 2011); provides more accurate spatial discrimination due to virtually

133

continuous sampling (Brown et al. 2002, Godet et al. 2009) and is non-destructive which is

134

important when surveying protected habitats and species (De Backer et al. 2009).

135

High costs and limited depth range restrict the use of both airborne sensing and satellite

136

imagery in marine habitat mapping at present although advances in hyperspectral mapping

6

137

should be reviewed in the future (Kenny et al. 2003, Brown et al. 2011). Acoustic sensing

138

has been used extensively in subtidal environments as a predictive tool, validated by

139

rigorous groundtruthing to confirm the results (Birkett et al. 1998, Hiscock 1998, Brown et

140

al. 2005, Ehrhold et al. 2006). There are four broad categories of acoustic mapping device:

141

(i) broad acoustic beam systems such as side scan sonar (SSS); (ii) acoustic ground-

142

discrimination systems such as RoxAnnTM and QTC-ViewTM (iii) multiple narrow-beam swath

143

bathymetric systems and (iv) multiple-beam side scan sonar (Kenny et al. 2003).

144 145

Main types of acoustic survey method for benthic habitat mapping

146 147

Side scan sonar

148

Broad beam swath systems such as side scan sonar can produce an almost photographic

149

representation of the seabed (JNCC 2001, Kenny et al. 2003, Georgiadis et al. 2009).

150

Comprising of an underwater transducer connected by a cable to the towing vessel where

151

data is recorded, an acoustic signal is emitted from a single beam or multiple beams rapidly

152

returning echoes which are transmitted to the recording device for later analysis (JNCC

153

2001). As the sonar is towed at a fixed height above the seabed, it casts relatively large

154

acoustic shadows enabling the detection of variations in sediment structure (Kenny et al.

155

2003). Side scan sonar provides continuous coverage of the area being surveyed (Brown et

156

al. 2011). The introduction of digital side scan sonar devices has increased mapping

157

capabilities with object detection possible down to tens of centimetres (JNCC 2001). To

158

some extent, the quality of the images generated can be evaluated manually with features

159

such as sand ripples identifiable by eye (JNCC 2001). The REBENT monitoring network in

7

160

France has adopted side scan sonar as part of its benthic mapping programme which

161

includes maerl beds (Ehrhold et al. 2006). Georgiadis et al. (2009) used side scan sonar to

162

map coralline algae in the southern Aegean Sea.

163

studies by Brown et al. (2002, 2005) and Freitas et al. (2006) to identify different seabed

164

assemblages alongside groundtruthing exercises and OSPAR recommends its application

165

where maerl beds are thick and extensive (OSPAR 2010).

Side scan sonar has also been used in

166 167

Acoustic ground-discrimination systems (AGDS)

168

Acoustic ground-discrimination systems (AGDS) operate using a hull-mounted single-beam

169

echosounder which detects differences in the seabed using acoustic reflection properties

170

(Greenstreet et al. 1997, Kenny et al. 2003). A single pulse is emitted from the device which

171

is directed straight down towards the seabed producing a footprint of the area directly

172

below the vessel (Brown et al. 2005). On reflection, the echo is returned to a transducer

173

(JNCC 2001).

174

discrimination systems do not produce continuous coverage maps like side scan sonar, but

175

instead produce a track covering the area beneath the vessel (Wilding et al. 2003). Gaps

176

between the tracks must be interpolated which can result in inaccurate assumptions about

177

the seabed habitat (Kenny et al. 2003, Brown et al. 2005). This means that AGDS should be

178

considered a predictive tool rather than a definitive view of the seabed (JNCC 2001, Wilding

179

et al. 2003). There are two systems commonly in use in the UK - RoxAnnTM and QTC-ViewTM

180

(JNCC 2001, Foster-Smith & Sotheran 2003). RoxAnnTM derives its values from the

181

interpretation of two elements of the returning echo: the first echo (E1) is related to

182

seafloor roughness, while the second multiple return echo (E2) is related to the hardness of

183

the seabed (Kenny et al. 2003, Wilding et al. 2003). Supplemented by groundtruthing, the

Due to the focused pulse emitted from the sounder, acoustic ground-

8

184

returned responses are classified into seabed characteristics (Kenny et al. 2003, Wilding et

185

al. 2003, Brown et al. 2005). QTC-ViewTM converts the echo into a digital form using the first

186

returning signal only and organises the seabed into acoustic classes (JNCC 2001, Ellingsen et

187

al. 2002).

188

considerable groundtruthing using calibration sites, the second relying on post-processing

189

analysis (Ellingsen et al. 2002). The use of AGDS has become widespread in SACs in the UK

190

(Brown et al. 2005) with Davies & Sotheran (1998) adopting this approach when evaluating

191

biotopes in Falmouth Bay and the lower Fal Ruan Estuary. The JNCC Marine Monitoring

192

Handbook (2001) recommends the use of AGDS where broad-scale surveys are required and

193

as a tool for locating sites of particular interest, thus reducing survey time. The cost of AGDS

194

in comparison to other acoustic devices is relatively cheap and integration with other

195

onboard systems such as GPS is straightforward (Birkett et al. 1998, Kenny et al. 2003,

196

Wilding et al. 2003). However, concerns have been raised around the unpredictability of

197

responses, resolution at varying depths, levels of interpolation required and accuracy when

198

determining habitat boundaries (Kenny et al. 2003, Wilding et al. 2003, Brown et al. 2005;

199

Freitas et al. 2011).

It can used in ‘supervised’ or ‘unsupervised’ modes, the first requiring

200 201

Multibeam echosounders

202

Multibeam echosounders (MBES) were originally an extension of single-beam

203

echosounders, transmitting multiple beams which are capable of covering a broad swath

204

either side of the vessels track (Brown & Blondel 2009, Simons & Snellen 2009). Multibeam

205

echosounding is becoming increasingly utilised within the field of seabed habitat mapping

206

due to its collective ability to obtain bathymetry and backscatter data concurrently (Brown

207

& Blondel 2009, Brown et al. 2011). The return signal can provide details of the geoacoustic 9

208

properties of the sea bed including grain size and porosity, both of which could be useful

209

features for identifying maerl beds (Brown & Blondel 2009). With the introduction of faster

210

processing capabilities and quality improvements to the backscatter images which are now

211

comparable to those collected through side scan sonar, studies using multibeam

212

echosounders have rapidly increased (Brown et al. 2011). Like side scan sonar, continuous

213

coverage maps can be created in conjunction with groundtruthing (Simons & Snellen 2009).

214

Brown & Blondel (2009) observed that multibeam echosounders are now able to provide as

215

much if not more information than side scan sonar. However, a high level of understanding

216

is required to establish the most appropriate analytical approach and significant expertise is

217

needed to interpret the data (Brown et al. 2011). To date no studies have been published

218

demonstrating the successful application of multibeam echosounders to identify maerl.

219

A more comprehensive review of acoustic techniques used for seabed habitat mapping can

220

be found in Brown et al. (2011).

221 222

Groundtruthing

223

While acoustic surveys are increasingly used to map and classify seabed habitats,

224

groundtruthing is still necessary either for calibration with acoustic analytical tools or to

225

enable classification of the discrete characteristics identified through acoustic imaging (JNCC

226

2001, Brown et al. 2011). Grab samples, towed or drop-down video and remote operated

227

vehicles (ROVs) are common methods of groundtruthing.

228 229

Grab samples

10

230

Grab sampling involves the use of a two shelled steel device that is lowered open to the

231

seabed and digs into the sediment, bringing the two shells together to retain a sediment

232

sample which can be analysed at the surface. There are a number of grab samples in

233

standard use: the van Veen which is most appropriate for soft sediments; the Day Grab

234

which can be used on a variety of sediment types and the Hamon Grab which can be used to

235

collect samples on coarser sediments including cobbles (JNCC 2001). Both the van Veen and

236

Day Grab devices can be used from a small vessel with two operators where the Hamon

237

Grab sampler can only be launched from a larger vessel and requires a minimum of three

238

operators (JNCC 2001).

239

consideration should be given to the method of sampling arrays.

240

Monitoring Handbook (2001) has details on random, stratified random and systematic

241

approaches to sampling. Analysis of the contents of the grab can be used to assist with the

242

classification of seabed characteristics found during acoustic surveys (Greenstreet et al.

243

1997, Davies & Sotheran 1998, Brown et al. 2002, Foster-Smith & Sotheran 2003, Freitas et

244

al. 2003, Ehrhold et al. 2006, Georgiadis et al. 2009). The number of samples and replicates

245

collected should take into consideration the area of the survey and the variations detected

246

from the acoustic mapping exercise (JNCC 2001).

When using grab sampling to groundtruth acoustic data, The JNCC Marine

247 248

Underwater video imaging

249

Boat operated underwater video imaging systems include drop-down video, towed sledge

250

video and remotely operated vehicles. Drop-down video involves the use of a video camera

251

attached to an umbilical cord being lowered over the side of the survey vessel either when

252

stationary or at low speed (JNCC 2001). This method gives the operator a limited degree of

253

control about the location studied and can be easily deployed to survey as many areas as 11

254

required (JNCC 2001). Brown et al. (2002) and Ehrhold et al. (2006) used drop-down video

255

to validate acoustic survey data collected for biotope mapping. Towed sledge video involves

256

a camera and lights mounted onto a rigid sled supported by buoyancy devices to keep the

257

image stable as the gear is towed (JNCC 2001). Large areas can be surveyed rapidly using

258

this approach and the clarity of the image enables accurate identification of biotopes (JNCC

259

2001). To reduce positional errors when comparing acoustic data to the video footage, a

260

transponder should be ideally fitted to the sledge to pinpoint its location (JNCC 2001).

261

Without a transponder, manual calculations will have to be performed prior to comparison.

262

Davies & Sotheran (1998) and Ruiz-Frau et al. (2007) used towed video when mapping

263

biotopes in the Fal. Remotely operated vehicles (ROVs) are also linked to the research vessel

264

by an umbilical cord but can be manoeuvred remotely by an operator onboard. ROVs can

265

survey large areas and focus on precise points of interest and are useful at sites with rapid

266

depth changes (Moore & Bunker 2001). However they are expensive and difficulties can be

267

encountered with recording the devices position. Georgiadis et al. (2009) used ROV drops in

268

conjunction with side scan sonar to map coralligène formations in the eastern

269

Mediterranean Sea and Thomson (2003) used an ROV as part of project to develop

270

autonomous sensors for marine resource mapping. All of these approaches provide a

271

permanent record of the seabed which can be stored, edited and reused. They are also

272

non-intrusive methods for identifying different substrate types. Successful use of any image

273

recording device is highly dependent on underwater visibility.

274 275

Evaluating proportions of live and dead maerl

276

12

277

Both live and dead maerl are considered important habitats for a diverse range of organisms

278

although the biodiversity on live maerl beds is considered greater (Birkett et al. 1998). The

279

slow growth rate of maerl means that any detrimental influences such as eutrophication,

280

invasive species, dredging or pollution is likely to have long-term implications for maerl and

281

its inhabitants (Hall-Spencer & Moore 2000, Barbera et al. 2003, Grall & Hall-Spencer 2003).

282

By establishing and monitoring the location and extent of live maerl beds, managers of the

283

Fal & Helford SAC will be able to observe any reduction in area.

284 285

There are a number of methods that could be used to collect this information. Grabs or

286

core samples (discussed above) could be used but would only provide data on a small

287

proportion of the survey area. They would also be unable to provide a quantitative

288

measurement as the grabs take a significant ‘bite’ from the seabed and the proportions of

289

sediment may not represent the actual quantity of live maerl present (Ruiz-Frau et al. 2007).

290

The use of drop-down or towed sledge video means that large areas can be surveyed

291

relatively quick to assess the extent of a live maerl bed but quantification of results would

292

again be difficult (Davies & Sotheran 1995, Ruiz-Frau et al. 2007). Thomson (2003) found, as

293

part of the SUMARE programme (Survey of Marine Resources) to establish autonomous

294

sensors for identifying maerl, that the use of a greylevel histogram applied to video footage

295

identified unique signatures for live and dead maerl. Although time consuming, direct diver

296

observation using quadrats or transect lines could be employed and would provide

297

quantifiable data on percentages of dead and live maerl (Axelsson et al. 2008). In the

298

Republic of Ireland, SCUBA divers use direct propulsion vehicles to rapidly assess

299

percentages (OSPAR 2010). All these methods could be interpreted and used in mapping.

300 13

301

Assessing community structure / biodiversity

302

303

The complex structure of maerl brings a number of challenges when surveying the

304

biodiversity of maerl beds. Steller et al. (2003) classified the type of organisms associated

305

with maerl into three main categories:

306



Epibenthic: motile or sessile organisms living on the seabed.

307



Cryptofaunal: those organisms living within the natural cavities created by the lattice network of maerl.

308 309



Infaunal: those individuals living buried in the substrate.

310

The small size of many organisms found on maerl beds has implications for their

311

classification and any detailed studies require a high level of taxonomic expertise. Birkett et

312

al. (1998) recognised this as an issue and observed that identifying down to genus level

313

could still provide enough information to assess the health of the biotope. The size of

314

organisms also affects the types of survey that can be selected to gain sufficient quantitative

315

information on biodiversity. Diver surveys, hand-held video and still photographs can

316

provide data on conspicuous species but may miss smaller organisms. These methods

317

cannot be used to survey the cryptofauna and infauna. In order to obtain results for these,

318

samples must be collected and analysed ex situ. As maerl is slow growing, the quantity of

319

samples required when employing any intrusive survey techniques such as grab samples and

320

cores needs to be carefully considered. Maggs (1983) suggests that the minimum sub-

321

sample size should be where a 10% increase in the number of species in the sub-sample is

322

derived from a 10% increase in the area. Processing of samples must be appropriately

14

323

designed to ensure the preservation of organisms for analysis and successful capture across

324

the size range of organisms.

325 326

In situ diving surveys

327

Diver quadrat surveys can be used for recording epibenthic species found on maerl.

328

Quadrats come in a variety of sizes, commonly 1m2, 0.25m2 or 0.1m2 (JNCC 2001). For maerl,

329

a 0.25m2 grid quadrat would be a sensible choice for the size of organisms under survey. A

330

minimum of two suitably qualified divers descend a weighted shot line, which can be used

331

by the survey vessel to record location, and lay a transect in a pre-agreed direction. This

332

avoids potential bias by the divers once underwater to select areas that look ‘most

333

interesting’ (Eleftheriou & McIntyre 2005). The quadrat and transect line should be slightly

334

negatively buoyant so that it can rest on the seabed while the divers complete the survey

335

(Axelsson et al. 2008). Divers should have a standard survey form to record species and

336

abundance. The JNCC Marine Monitoring Handbook (2001) recommends conducting a pilot

337

survey of the location to familiarise the divers with the species likely to be encountered

338

during the survey. Once the survey is complete, the dive team should use a delayed surface

339

marker buoy to inform the survey vessel of the end location. This will enable the results to

340

be mapped. Collecting data in this way is a non-destructive technique; provides quantitative

341

data which allows changes to species composition to be monitored over time; is a simple

342

method for recording conspicuous species without damaging the maerl and is easily

343

repeatable (Eleftheriou & McIntyre 2005). The divers need to be confident of their buoyancy

344

control to avoid kicking up sediment or causing damage to the surrounding maerl; should

345

have an understanding of the biotope and potential species and have the appropriate

15

346

qualifications for conducting underwater surveys (JNCC 2001). Percentages of live and dead

347

maerl could also be recorded as part of this survey. Steller et al. (2003) used transect

348

surveys to estimate species richness and abundance on maerl beds in the Gulf of California.

349

Hand-held video surveys carried out by qualified divers can provide information on the

350

conspicuous benthos in the chosen study site (JNCC 2001). A video camera, mounted in

351

underwater housing and with lighting to improve image quality is the standard equipment

352

required (JNCC 2001). It provides a permanent record of the site surveyed and analysis can

353

be conducted ex situ. Poor underwater visibility; scaling of the images recorded; the ability

354

to collect quantitative data that can be readily related to GPS points and consistency of

355

recording means that this method may be more appropriate for collecting footage that can

356

be used for educational purposes rather than monitoring. Axelsson et al. (2008) conducted

357

diver video surveys in the Fal Estuary in conjunction with in situ diver observations.

358

Still photography of maerl beds involves the use of an underwater high-resolution camera

359

with lighting. In order to obtain quantitative data, the camera should be mounted onto a

360

reference frame or a quadrat used to provide a scale to the photograph (JNCC 2001). In the

361

same way as video, photographs provide a permanent record and with greater resolution

362

capabilities than video, photographs can enable more detailed images to be collected.

363

Analysis can be carried out ex situ meaning that the divers do not need to be taxonomists.

364

Most commonly used for collecting fixed point data, there are currently no examples of this

365

method being used for random sampling (JNCC 2001). However, this method could be used

366

in conjunction with a diving quadrat survey to record unidentified specimens or get close up

367

shots without removing specimens.

368 16

369

Sample collection techniques

370

Hand-held cores can be used to collect cryptic fauna, infauna and sediment samples

371

(Bordehore et al. 2003, Moore et al. 2004, Axelsson et al. 2008, Sciberras et al. 2009). These

372

cores are operated by divers who manually push the core into the sediment. Axelsson et al.

373

(2008) found that the substrate in areas of the Fal made the extraction of sediment samples

374

using hand-held cores quite challenging. On reaching the appropriate depth, the top and

375

bottom of the corer are sealed with caps and it is placed into bags for secure storage and to

376

prevent any organisms escaping (Axelsson et al. 2008, Sciberras et al. 2009). Ideally on

377

board the survey vessel and within 24 hours of collection, the samples should be sieved and

378

fixed in 10% formal saline to ensure the samples are preserved for laboratory analysis (JNCC

379

2001, Axelsson et al. 2008). The small nature of some species found on maerl means that

380

the mesh size should be below 1000Îźm to ensure robust analysis (Moore et al. 2004,

381

Axelsson et al. 2008).

382

To collect cryptic fauna, Steller et al. (2003) used divers to collect random samples of maerl

383

thalli by hand, which were then preserved and the cryptic and burrowing species were

384

extracted in the laboratory for analysis.

385

Grab samples (discussed in the mapping section) can be used for biological sampling as well

386

as groundtruthing (Sciberras et al. 2009). A combined approach to groundtruthing and

387

infaunal sample collection can involve skimming off the top layer of the contents of the grab

388

sample for sediment analysis and fixing the rest for biological analysis in the laboratory

389

(Moore et al. 2004). Ruiz-Frau et al. (2007) used a 0.1m2 Day Grab for collecting sediment

390

and biological samples in Falmouth Bay. Grab samplers usually require deployment from a

391

research vessel with space to winch the samples in.

17

392

393

Measuring abiotic factors that could impact the health of maerl beds

394

Environmental tolerances of maerl are still poorly understood (Birkett et al. 1998). However,

395

any robust monitoring programme should include abiotic measurements so they can be

396

factored in if any unexplained degradation of the maerl beds occurs.

397

Temperature is known to affect the geographic distribution of maerl beds with L.

398

corallioides absent in Scotland due to cooler temperatures but present in southwest Britain

399

(Birkett et al. 1998, Wilson et al. 2004). The species composition of maerl beds is influenced

400

by temperature, so monitoring the water temperature on maerl beds could track changes

401

that may occur as a result of climate change (Wilson et al. 2004). Maerl beds are normally

402

found in fully saline conditions but the impact of variable salinity conditions is not

403

understood (Birkett et al. 1998). Temperature and salinity can be measured together in situ

404

using a temperature-salinity probe (Sciberras et al. 2009); through the use of a CTD

405

(conductivity-temperature-depth) package or by using a niskin bottle to collect water

406

samples for analysis on the surface.

407

Maerl is a coralline algae and therefore needs to photosynthesise in order to grow, however

408

irradiance requirements are not understood for maerl (Birkett et al. 1998). In the UK, maerl

409

beds rarely exceed 30m (Wilson et al. 2004). Turbidity can affect the amount of light

410

penetrating to the maerl bed and can be measured simply using a secchi disk (Sciberras et

411

al. 2009).

412

The nutrient requirements of maerl are not known, however with a rigid skeleton of calcium

413

carbonate maerl does have a requirement for calcium (Birkett et al. 1998). In laboratory 18

414

experiments, King & Scramm (1982) found that the calcium ionic concentration affected

415

maerl growth, with an optimum uptake of 30 ‰. Under laboratory conditions, Martin &

416

Gatuzzo (2009) conducted experiments to assess the effects of ocean acidification on

417

coralline algae and found that based on current projections, net dissolution was likely to

418

exceed net calcification in Lithothamnion cabiochae by the end of the century. pH therefore

419

should be monitored and can be tested in situ using an underwater housed pH meter or on

420

the research vessel if a water sample has been collected.

421

422

Discussion

423

424

The three-dimensional structure of maerl brings additional complexities and considerations

425

on top of those encountered during other subtidal surveys. The current deficiency in

426

standardised protocols for assessing maerl communities combined with rapid advances in

427

the technology used for mapping benthic habitats makes difficult work for conservation

428

managers when establishing a monitoring programme. There is no single method that can

429

monitor all the conservation objectives set for maerl within the Fal & Helford SAC. Instead

430

the solution requires a suite of approaches that will satisfy the requirements and provide

431

the management team with a robust dataset that can inform decision-making.

432

recommendations discussed in the proceeding sections are based on the knowledge gained

433

through studies on maerl in other regions, the use of standardised methodologies where

434

possible and factor in resource and cost considerations.

435

sensitivities of maerl, the recommendations exhibit a preference towards non-destructive

436

techniques where feasible. Table 1 summarises the recommendations discussed below.

19

The

Due to the environmental

437

438

Recommendations for mapping

439

While the importance and potential application of acoustic devices for seabed habitat

440

mapping is widely recognised, the difficulties with accurately differentiating maerl habitats

441

from other mixed sediments is still problematic and can currently only be used if validated

442

with groundtruthing. All three forms of acoustic sensing discussed have been used to map

443

maerl biotopes but the most recent research shows a preference towards the use of side

444

scan sonar in conjunction with a multibeam echosounder (Kenny et al. 2003, Diaz et al.

445

2004, Ehrhold et al. 2006, Brown et al. 2011). Side scan sonar has the highest definition of

446

seabed features amongst the techniques in use and this combined with the bathymetric and

447

backscatter imaging provided by multibeam echosounders will generate a robust baseline

448

for the monitoring programme (Diaz et al. 2004). The two devices are also capable of

449

providing 100% coverage unlike AGDS which needs interpolation between the tracks. From

450

previous studies of maerl in the Fal Estuary, it is apparent that maerl occurs in fairly shallow

451

waters (Blundel et al. 1981, Hiscock 1998). Acoustic surveys therefore need to be carried

452

out during high tides for maximum accuracy. Provision will need to be made within the

453

budget for a mapping expert to advise on the survey design and interpret the outputs. Due

454

to the area the Fal & Helford SAC covers, the quickest and most cost-effective option for

455

groundtruthing is drop-down video. For deeper parts like the channel in Carrick Roads,

456

towed sledge video may be required but will give comparable results.

457 458

While these surveys can be carried out at any point during the year, it is recommended that

459

mapping is carried out during the summer months when visibility, light and weather

20

460

conditions are optimum. For consistency, future surveys should be carried out across the

461

same period. Surveys lasting longer than an hour should have tidal corrections applied

462

(Brown et al. 2005).

463 464

Recommendations for evaluating proportions of live and dead maerl

465

An initial baseline assessment should focus on establishing the location and dimensions of

466

the live maerl beds. Drop-down video is a practical way to collect this data and would work

467

well with the groundtruthing exercise. With drop-down video, GPS points can be easily

468

collected when live maerl is observed and later plotted onto a GIS map. Where live maerl

469

beds are identified surveys should be conducted to identify the perimeter of the bed so that

470

a true area can be calculated. While the primary goal is to obtain a map showing the

471

locations, another important measurement is to identify the proportion of live and dead

472

maerl present within the live maerl beds. The best method for obtaining quantitative data

473

is to conduct diver quadrat surveys along a series of transects. Procedural Guideline 3-7

474

from the JNCC Marine Monitoring Handbook (2001) covers the methodology in more detail.

475

Measurements should be taken as percentages not abundance scales to enable quantitative

476

analysis. It should be noted that these survey methods will only measure the surface layer

477

of the maerl.

478

479

Recommendations for biodiversity

480

Apart from the maerl species there are no key indicator species associated with maerl at

481

present so it is necessary to ensure a robust biodiversity survey is conducted. Collecting data

21

482

on the number and type of species found on maerl beds will require the application of

483

several methodologies and is likely to be the most time-consuming part of the monitoring

484

programme. Both live and dead maerl deposits should be surveyed. Multiple diver quadrat

485

surveys along a transect line are recommended for surveying the epifauna and flora

486

following the sample size recommendations proposed by Maggs (1983). This approach will

487

require at least one diver to be a trained biologist with an understanding of the taxonomy of

488

organisms associated with maerl. Organisms should be identified down to species level

489

where possible but genus is acceptable. The second diver should have a high-resolution

490

underwater camera with a macro setting and strobe lighting. Each quadrat should be

491

photographed with a unique id. Any unknown organisms should be photographed for

492

identification ex situ. The photograph should include a scale for reference. A standard form

493

should be generated for the survey team to complete including depth, temperature and

494

percentage of live and dead maerl. Any diving surveys must comply with the Diving at Work

495

Regulations 1997 and adhere to the Scientific and Archaeological Approved Code of

496

Practice.

497 498

There are currently no non-destructive methods for surveying the infauna. The use of a

499

diver hand-held corer is considered a suitable method for obtaining samples. A number of

500

objectives can be achieved through collecting core samples. The species of maerl will be

501

easier to identify in the laboratory, the underlying sediment can be measured and cryptic

502

fauna and infauna can be surveyed at the same time. Samples should be processed and

503

fixed within 24 hours of collection for later analysis in a laboratory. Comprehensive

504

methodologies for collecting, processing and analysing cryptic fauna and infauna can be

505

found in Steller et al. (2003) and Sciberras et al. (2009) respectively.

22

506 507

Due to the seasonal variations experienced on maerl beds, two sampling seasons are

508

recommended to gain a greater understanding of community change however this will be

509

constrained by the budget allotted to the monitoring programme. Consideration should

510

also be given to avoid extensive destructive survey techniques around any peak recruitment

511

periods. If only one survey is practicable, then July is advised when species richness is at its

512

peak yet recruitment and settlement of known commercially important species is low

513

(Kamenos et al. 2004b, c, PeĂąa & BĂĄrbara 2010).

514 515

Recommendations for measuring abiotic factors

516

Although OSPAR (2010) states that monitoring should be conducted as a minimum at six-

517

yearly intervals for SACs, it is recommended that abiotic factors should be collected twice

518

yearly during Spring and Autumn. Plankton levels are generally high in Spring while water

519

temperature is at its annual lowest, conversely in late Autumn, annual water temperature

520

reaches its maximum and plankton is on the decline (Miller 2004). Temperature, salinity,

521

pH, turbidity and dissolved oxygen levels should be recorded. These are relatively simple

522

and quick measurements to collect and may be important if any change to the extent and

523

distribution of the maerl is observed. It is important that the same equipment is used and

524

calibrated each time thus avoiding potential discrepancies between devices.

525

526

Further recommendations

23

527

Continuing advances in the technology surrounding benthic habitat mapping and our

528

increasing understanding of maerl biotopes mean that the techniques recommended in this

529

review will need to be reassessed at appropriate junctures.

530

While not within the scope of the review, it is worth emphasising the importance of the

531

supporting systems that will need to be established in order to manage and store the data

532

collected through the monitoring programme. A suitable format will need to be selected

533

which is likely to include GIS functionality and scope for statistical analysis of the data.

534

535

Conclusions

536

537

The high biodiversity associated with maerl beds has long been recognised. However for

538

many years maerl has been subjected to damaging anthropogenic activities such as

539

aggregate extraction and dredging. Investigations on maerl have largely focused on

540

assessing the implications of these destructive processes or sought to gain a greater

541

understanding of the biology and ecology associated with maerl. As such, there have been

542

few monitoring programmes established to look at the long-term dynamics of maerl bed

543

communities.

544

Valuable contributions have been made by the scientific community to expand our

545

understanding of maerl. These studies have shown that maerl grows exceptionally slowly,

546

has narrow environmental tolerances and is highly sensitive to disturbance resulting in the

547

acknowledgement that maerl is a non-renewable resource. They have also identified its role

548

in carbon sequestration and as a nursery ground for commercially important species.

24

549

As a consequence, a growing emphasis is being placed on the conservation importance of

550

maerl beds, with local and European protection designations at both species and habitat

551

level.

552

comprehensive baseline from which to monitor long-term trends.

553

Those parties involved in the management of the Fal & Helford SAC should find this review a

554

useful summary of the techniques most suitable for surveying maerl beds. While it shows

555

that establishing a maerl monitoring programme for the Fal & Helford SAC is a complex

556

process that will involve significant time, cost and planning, it also demonstrates that there

557

are multiple methods that can be adopted in order to achieve the primary conservation

558

objectives.

In order to manage maerl beds effectively, it is important to establish a

559

560

Acknowledgements

561

562

This review was kindly supported by the Falmouth Harbour Commissioners. This manuscript

563

benefited from comments by C. Eatock, A. O’Brien, T. Russell, and A. Thornton. Particular

564

thanks go to thank N. Woods for his assistance with testing ROV and multibeam

565

echosounder methodologies and the use of the research vessel RV Ann Kathleen.

566

567

References

568

25

569

Axelsson M, Bamber R, Dewey D, Duke S, Hollies R (2008) Marine ecological survey. In:

570

Falmouth Cruise Project Environmental Impact Assessment

571

Barbera C, Bordehore C, Borg JA, Glémarec M, Grall J, Hall-Spencer JM, De la Huz CH,

572

Lanfranco E, Lastra M, Moore PG, Mora J, Pita ME, Ramos-Esplá AA, Rizzo M, Sánchez-Mata

573

A, Seva A, Schembri PJ, Valle C (2003) Conservation and management of northeast Atlantic

574

and Mediterranean maerl beds. Aquat Conserv 13:65-76

575

Birkett DA, Maggs CA, Dring MJ (1998) An overview of dynamic and sensitivity

576

characteristics for conservation management of marine SACs, vol 5. Maerl, [UK Marine SACs

577

Project], Scottish Association for Marine Science, Scotland, 116 pp.

578

Blunden G, Farnham WF, Jephson N, Barwell CJ, Fenn RH, Plunkett BA (1981) The

579

composition of maerl beds of economic interest in Northern Brittany, Cornwall and Ireland.

580

Proceeds of the International Seaweed Symposium 10:651-656

581

Bordehore C, Ramos-Esplá AA, Riosmena-Rodríguez R (2003) Comparative study of two

582

maerl beds with different otter trawling history, southeast Iberian Peninsula. Aquat Conserv

583

13:43-54

584

Bosence D, Wilson J (2003) Maerl growth, carbonate production rates and accumulation

585

rates in the northeast Atlantic. Aquat Conserv 13:21-31

586

Brown CJ, Blondel P (2009) Developments in the application of multibeam sonar backscatter

587

for seafloor habitat mapping. Applied Acoustics 70:1242-1247

26

588

Brown CJ, Cooper KM, Meadows WJ, Limpenny DS, Rees HL (2002) Small-scale mapping of

589

sea-bed assemblages in the eastern English Channel using sidescan sonar and remote

590

sampling techniques. Est Coast Shelf Sci 54:263-278

591

Brown CJ, Mitchell A, Limpenny DS, Robertson MR, Service M, Golding N (2005) Mapping

592

seabed habitats in the Firth of Lorn off the west coast of Scotland: evaluation and

593

comparison of habitat maps produced using the acoustic ground-discrimination system,

594

RoxAnn, and sidescan sonar. ICES J Mar Sci 62:790-802

595

Brown CJ, Smith SJ, Lawton P, Anderson JT (2011) Benthic habitat mapping: a review of

596

progress towards improved understanding of the spatial ecology of the seafloor using

597

acoustic techniques. Est Coast Shelf Sci 92:502-520

598

Canals M, Ballesteros E (1997) Production of carbonate particles by phytobenthic

599

communities on the Mallorca-Menorca shelf, northwestern Mediterranean Sea. Deep-Sea

600

Res Part II 44:611-629

601

Challinor S, Solly N, Baugh J, Adnitt C, Hillyer K, Covington L, Velterop R, Drabble J, Potts M,

602

Thornton P, Birch T (2009) Commercial fisheries and shellfisheries. Port of Falmouth

603

Development Initiative

604

Davies J, Baxter J, Bradley M, Connor D, Khan J, Murray E, Sanderson W, Turnbull C, Vincent

605

M (2001) Marine Monitoring Handbook, 405 pp

606

Davies J, Sotheran I (1995) Mapping the distribution of benthic biotopes in Falmouth Bay

607

and the lower Fal Ruan Estuary. English Nature Research Report No 119a

27

608

De Backer A, Adam S, Monbaliu J, Toorman E, Vincx M, Degraer S (2009) Remote sensing of

609

biologically reworked sediments: a laboratory experiment. Estuaries and Coasts 32:1121-

610

1129

611

De Grave S, Fazakerley H, Kelly L, Guiry MD, Ryan M, Walshe J (2000) A study of selected

612

maĂŤrl beds in Irish waters and their potential for sustainable extraction. Marine Institute

613

De Grave S, Whitaker A (1999) A census of maerl beds in Irish waters. Aquatic Conservation:

614

Marine and Freshwater Ecosystems 9:303-311

615

Diaz RJ, Solan M, Valente RM (2004) A review of approaches for classifying benthic habitats

616

and evaluating habitat quality. J Environ Manage 73:165-181

617

Ehrhold A, Hamon D, Guillaumont B (2006) The REBENT monitoring network, a spatially

618

integrated, acoustic approach to surveying nearshore macrobenthic habitats: application to

619

the Bay of Concarneau (South Brittany, France). ICES J Mar Sci 63:1604-1615

620

Eleftheriou A, McIntyre AD (2005) Methods for the study of marine benthos. Blackwell

621

Science Ltd, Oxford

622

Ellingsen KE, Gray JS, Bjørnbom E (2002) Acoustic classification of seabed habitats using QTC

623

VIEWTM system. ICES J Mar Sci 59:825-835

624

Foster MS (2001) Rhodoliths: between rocks and hard places. J Phycol 37:659-667

625

Foster-Smith R, Connor D, Davies J (2007) MESH guide to habitat mapping. Mapping

626

European Seabed Habitats.

627

Foster-Smith RL, Sotheran IS (2003) Mapping marine benthic biotopes using acoustic ground

628

discrimination systems. Int J Remote Sens 24:2761-2784 28

629

Freitas R, Rodrigues AM, Quintino V (2003) Benthic biotopes remote sensing using acoustics.

630

J Exp Mar Biol Ecol 285-286:339-353

631

Freitas R, Sampaio L, Oliveira J, Rodrigues AM, Quintino V (2006) Validation of soft bottom

632

benthic habitats identified by single-beam acoustics. Mar Pollut Bull 53:72-79

633

Freitas R, Ricardo F, Pereira F, Sampaio L, Carvalho S, Gaspar M, Quintino V, Rodrigues AM

634

(2011) Benthic habitat mapping: concerns using a combined approach (acoustic, sediment

635

and biological data Est Coast Shelf Sci 92:598-606

636

Georgiadis M, Papatheodorou G, Tzanatos E, Geraga M, Ramfos A, Koutsikopoulos C,

637

Ferentinos G (2009) Coralligène formations in the eastern Mediterranean Sea: morphology,

638

distribution, mapping and relation to fisheries in the southern Aegean Sea (Greece) based

639

on high-resolution acoustics. J Exp Mar Biol Ecol 368:44-58

640

Godet L, Fournier J, Toupoint N, Oliver F (2009) Mapping and monitoring intertidal benthic

641

habitats: a review of techniques and a proposal for a new visual methodology for the

642

European coasts. Progress in Physical Geography 33:378-402

643

Grall J, Glémarec M (1997) Biodiversité des fonds de maerl en Bretagne: approche

644

fonctionnelle et impacts anthropogeniques. Vie et Milieu 47(4):339-349

645

Grall J, Hall-Spencer JM (2003) Problems facing maerl conservation in Brittany. Aquat

646

Conserv 13:55-64

647

Greenstreet SPR, Tuck ID, Grewar GN, Armstrong E, Reid DG, Wright PJ (1997) An

648

assessment of the acoustic survey technique, RoxAnn, as a means of mapping seabed

649

habitat. ICES J Mar Sci 54:939-959

29

650

Hall-Spencer JM (2005) Ban on maerl extraction. Mar Pollut Bull 50:121

651

Hall-Spencer JM, Kelly J, Maggs CA (2010) OSPAR Background document for maerl beds.

652

Department of the Environment, Heritage & Local Government, Ireland

653

Hall-Spencer JM, Moore PG (2000) Scallop dredging has profound, long-term impacts on

654

maerl habitats. ICES J Mar Sci 57:1407-1415

655

Held A, Ticehurst C, Lymburner L, Williams N (2003) High resolution mapping of tropical

656

mangrove ecosystems using hyperspectral and radar remote sensing. Int J Remote Sens

657

24:2739-2759

658

Hiscock K (1998) Biological monitoring of marine special areas of conservation: a review of

659

methods for detecting change. Part 1. Review and description of methods. Consultation

660

draft. Joint Nature Conservation Committee, Peterborough.

661

Kamenos NA, Moore PG, Hall-Spencer JM (2004c) Maerl grounds provide both refuge and

662

high growth potential for juvenile queen scallops (Aequipecten opercularis L.). Journal J Exp

663

Mar Biol Ecol 313:241-254

664

Kamenos NA, Moore PG, Hall-Spencer JM (2004b) Nursery-area function of maerl grounds

665

for juvenile queen scallops Aequipecten opercularis and other invertebrates. Mar Ecol Prog

666

Ser 274:183-189

667

Kamenos NA, Moore PG, Hall-Spencer JM (2004d) Small-scale distribution of juvenile

668

gadoids in shallow inshore waters; what role does maerl play? ICES J Mar Sci 61:422-429

669

Kamenos NA, Moore PG, Hall-Spencer JM (2004a) Substratum heterogeneity of dredged vs

670

un-dredged maerl grounds. J Mar Biol Ass UK 83:411-413 30

671

Kamenos NA, Moore PG, Stevenson TGI (2004) Marine survey to identify maerl beds:

672

Lamlash Bay Long Sea Outfall. University Marine Biological Station Millport, Isle of Cumbrae

673

Kenny AJ, Cato I, Desprez M, Fader G, SchĂźttenhelm RTE, Side J (2003) An overview of

674

seabed-mapping technologies in the context of marine habitat classification. ICES J Mar Sci

675

60:411-418

676

King RJ, Schramm W (1982) Calcification in the maerl coralline alga Phymatolithon

677

calcareum, effects of salinity and temperature. Marine Biology 70:197–204

678

Maggs CA (1983) A seasonal study of seaweed communities on subtidal maerl (unattached

679

coralline algae). Progress in Underwater Science 9:27-40

680

Malthus TJ, Karpouzli E (2003) Integrating field and high spatial resolution satellite-based

681

methods for monitoring shallow submersed aquatic habitats in the South of Eriskay,

682

Scotland, UK. Int J Remote Sens 24:2585-2593

683

Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean

684

acidification and elevated temperature. Global Change Biology 15:2089-2100

685

Meadows B, Limpenny D, Eggleton J, Foster-Smith RL (2006) Case study: optimal detection

686

and identification of biogenic structures using side scan sonar. Mapping European Seabed

687

Habitats

688

Miller CB (2004) Biological oceanography. Blackwell Publishing, Oxford

689

Moore J, Bunker F (2001) Development of methods for monitoring subtidal biotope extent

690

using remote video. JNCC Report No 369

31

691

Moore CG, Lyndon AR, Mair JM (2004) The establishment of site condition monitoring of

692

marine sedimentary habitats in the Sound of Arisaig cSAC. Scottish Natural Heritage

693

Commissioned Report No. 071

694

Peña V, Bárbara I (2010) Seasonal patterns in the maërl community of shallow European

695

Atlantic beds and their use as a baseline for monitoring studies. Eur J Phycol 45:327-342

696

Perrins JM, Bunker F, Bishop GM (1995) A comparison of the maerl beds of the Fal Estuary

697

between 1982 and 1992. Report to English Nature

698

Ruiz-Frau A, Rees EIS, Hinz H, Kaiser MJ (2007) Falmouth Bay maerl community benthic

699

survey. University Of Wales Bangor, Wales

700

Sciberras M, Rizzo M, Mifsud JR, Camilleri K, Borg JA, Lanfranco E, Schembri PJ (2009)

701

Habitat structure and biological characteristics of a maerl bed off the northeastern coast of

702

the Maltese Islands (central Mediterranean). Marine Biodiversity 39:251-264

703

Simons DG, Snellen M (2009) A Bayesian approach to seafloor classification using multi-

704

beam echo-sounder backscatter data. Applied Acoustics 70:1258-1268

705

Steller DL, Riosmena-Rodríguez R, Foster MS, Roberts CA (2003) Rhodolith bed diversity in

706

the Gulf of California: the importance of rhodolith structure and consequences of

707

disturbance. Aquat Conserv 13:5-20

708

Thomson M (2003) Summary report to possible end-users. Survey of Marine Resources

709

(SUMARE), Orkney

710

Wilding TA, Sayer MDJ, Provost PG (2003) Factors affecting the performance of the acoustic

711

ground discrimination system RoxAnnTM. ICES J Mar Sci Science 60:1373-1380 32

712

Wilson S, Blake C, Berges JA, Maggs CA (2004) Environmental tolerances of free-living

713

coralline algae (maerl): implications for European marine conservation. Biol Conserv

714

120:283-293

33