Wild gregarious settlements of Ostrea edulis in a semi‐enclosed Sea Lough; a case study for unassisted restoration
Smyth, D. M., Horne, N. S., Ronayne, E., Millar, R. V., Joyce, P. W. S., Hayden‐Hughes, M., & Kregting, L. (2020). Wild gregarious settlements of Ostrea edulis in a semi‐enclosed Sea Lough; a case study for unassisted restoration. Restoration Ecology. https://doi.org/10.1111/rec.13124
Published in: Restoration Ecology
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Download date:03. Oct. 2021 Ostrea edulis unassisted restoration
1 Wild gregarious settlements of Ostrea edulis in a semi-enclosed
2 Sea Lough; a case study for unassisted restoration
3
4 Running Head: Ostrea edulis unassisted restoration
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6 Authors and Address: David M. Smythad*, Nicholas S. Hornea, Elli Ronayneb, Rachel
7 V. Millara, Patrick W.S. Joyceac, Maria Hayden-Hughesc and Louise Kregtinga
8 a School of Natural and Built Environment, Queen's University Belfast, Northern
9 Ireland, United Kingdom
10 b Marine and Freshwater Research Centre (MFRC), Galway-Mayo Institute of
11 Technology, County Galway, Ireland
12 c Danish Shellfish Centre, DTU Aqua, Øroddevej 80, 7900 Nykøbing Mors, Denmark
13 * Correspondence address: d School of Ocean Science, Bangor University Wales,
14 LL59 5AB. E-mail:[email protected].
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16 Author Contributions: DS, LK conceived and designed the research; DS,LK,PJ
17 performed field surveys; DS,RM,NH,ER,MHH analysed the data; ER,RM,NH,LK
18 contributed materials/analysis tools; DS,LK,PJ wrote and edited the manuscript.
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26 Abstract
27 Ostrea edulis was once prolific throughout Europe and considered as the
28 continent’s native oyster. However, O. edulis currently exists in small fragmented
29 assemblages where natural unaided recovery is rarely encountered. This research
30 identified the small semi-enclosed sea lough of Strangford on the north east coast of
31 Northern Ireland as one of the few locations within Europe where the native oyster
32 displayed gregarious natural rejuvenation. On close examination, four influential
33 parameters appeared to assist in concentrated settlement; raised topographical cultch
34 formations, shell coverage, the number of fecund in-situ adult’s and site protection. If
35 these components were to be combined and managed as part of reintroduction and
36 restoration initiatives, high density settlements and self-sustaining populations may be
37 possible. The research also identified that unregulated harvesting of intertidal O. edulis
38 assemblages has the potential to seriously hinder natural recoveries. Indeed, the
39 findings suggest that a review of policy in regards to intertidal hand gathering is
40 necessary. However, naturally occurring high density settlements recorded during this
41 research should be inspirational to all involved in the restoration of the native oyster.
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43 Keywords; high density settlements, multiple attachments, native oyster, spatting
44 pools, unregulated harvesting
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Ostrea edulis unassisted restoration
51 Implications for Practice
52 • Examination of naturally occurring native oyster expansion and the
53 parameters which permit augmentation can provide an insight into which
54 components could be implemented to aid successful assisted restoration.
55 • A suite of abiotic and biotic conditions can accommodate mass gregarious
56 Ostrea edulis settlements; hydrodynamics which allow water retention,
57 adequate coverage of suitable substrate, intertidal topography which provides
58 pool structures, in-situ resident adults and policing of settlement sites.
59 • Unregulated harvesting remains a constant threat to restoration and
60 protection of the species needs to be implemented if a self-sustaining status is
61 to be achieved.
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63
64 Introduction
65 Oysters as a species have been important biogenic and economic components
66 within estuarine, coastal and offshore habitats throughout the world (Coen & Grizzle
67 2007). The immensity of their topographical coverage and economic productivity
68 supported communities for centuries (Trimble et al. 2009). The Roman philosopher
69 Pliny describes the extensive harvesting of oysters in Brittany, France by Sergius
70 Orata at Baiae in 95 BC (Günther 1897; Marzano 2013). In the Persian Gulf circa 250
71 AD Babylonian fishing fleets were commercially exploiting the pearl oyster Pinctada
72 radiata (Carter 2005). The Gulf fishery developed into a considerable financial concern
73 which was valued at £240,000 per annum in 1829, a figure which represents
74 >£25,000,000 today. However, heavy exploitation resulted in the fishery being
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75 economically non-viable by the late 1890s (Bowen 1951). Similarly, in the United
76 States of America during the mid-1800s, the Crassostrea virginica fishery was under
77 considerable strain (Kirby 2004). In 1869 the Maryland fishery landed >150,000 tonnes
78 of oysters worth $5,000,000, a current market equivalent of $80,000,000 (MacKenzie
79 2007). Likewise, in Europe in the mid-1800s, wild Ostrea edulis stocks were
80 undergoing a comparable level of exploitation (Eyton 1958). The scale of harvesting
81 was immense with shell piles at oyster shucking houses regularly containing >1 trillion
82 shells (Goulletquer & Heral 1997). The global demand for oysters led to the classic
83 overfishing scenario whereby demand outweighed resource, culminating in a
84 worldwide collapse of stocks by the early 1900s (Korringa 1946; Thurstan et al. 2013).
85 The rapid large-scale removal of these primary ecosystem components
86 resulted in several detrimental ecological consequences such as; a deterioration in
87 water quality, an increase in invasive pest species and a prevalence of new disease
88 (Conner & Simon 1979; Jackson et al. 2001). The anthropogenic removal of global
89 oyster reef ecosystems was almost total with an estimated 85% loss over the last 200
90 years accompanied with a legacy of 85% habitat loss (Beck et al. 2011).
91 Governments, habitat managers and Non-Governmental Organisations have
92 recognised and accepted that this loss has contributed to the accelerated deterioration
93 of the ecological health of numerous marine ecoregions. As a result, a consensus now
94 exists among concerned stakeholders that active restoration of oyster reefs should be
95 supported and encouraged whenever possible (Alleway & Connell 2015). Indeed, the
96 European Union has identified that biogenic oyster reefs under the Natura 2000 are
97 habitats which require immediate protection, augmentation and restoration (Bostock
98 et al. 2010). As the majority of historic European oyster sites are in a poor state of
99 conservational health, any locations which retain a resident self-sustaining population
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100 could offer an important insight into environmental parameters which could be
101 replicated to promote recovery (Carlucci et al. 2010). Presently numerous European
102 countries are attempting to address the dwindling wild stocks through the
103 augmentation of cultured or translocated oysters (Smyth et al. 2018; Pogoda et al.
104 2019).
105 Even though many European O. edulis populations are extremely fragmented
106 and in low densities, the fecundity and life cycle of the oyster suggest that when abiotic
107 and biotic parameters are optimal the potential for large scale recovery should be
108 possible (Taylor & Bushek 2008). However, rejuvenation within wild O. edulis
109 assemblages is rare with only a few remote sites displaying tentative recovery.
110 Nevertheless, those which do exist could offer valuable indicators as to what in-situ
111 conditions are required to reinstate or support a restored population (Laing et al. 2006;
112 Christianen et al. 2018). One such location worthy of investigation is the small, semi-
113 enclosed sea Lough of Strangford on the north east coast of Northern Ireland.
114 The native oyster fishery in Strangford Lough was once renowned throughout Ireland
115 for its abundant intertidal and subtidal beds (Day & McWilliams 1991). The
116 Montgomery Records of 1680 (Montgomery 1683) stated that, “the Strangford Lough
117 beds are dredged daily with oyster clumps gathered in deep water as well as on the
118 Lough shore”. Lewis (1837) when discussing the fishery referred to several sites that
119 were renowned for their productivity; Ringhaddy Sound, Cunningburn Milltown and
120 Greyabbey. However, even though Strangford possessed a significant oyster stock it
121 experienced the same overexploitation as the rest of Europe and was considered
122 functionally extinct by the early 1900s (Nunn 1994). Consequently only the occasional
123 solitary individual was recorded up until the late 1990s (Kennedy & Roberts 1999).
124 Though, in 1998 a single spawning event of an O. edulis aquaculture assemblage
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125 triggered an unintentional rejuvenation of the wild stock (Kennedy & Roberts 1999).
126 The spawning resulted in the Lough’s population growing from an estimated 100
127 individuals to > 1.5 million in a period of five years (Smyth et al. 2009). Unfortunately,
128 the rapid increase of wild oysters was accompanied by an upsurge in unregulated
129 commercial harvesting and over the following three years the population declined to
130 <400,000 (Smyth et al. 2009). Nonetheless, the potential for gregarious oyster
131 settlements within the Lough was established and a hydrodynamic larval tracking
132 model confirmed the north east coast as a potential O. edulis larval sink (Figure 1)
133 (Smyth et al. 2016).
134 The Lough has benefited from being studied since the early 1960s and is a
135 designated Marine Conservation Zone (Roberts et al. 2011). Intense trawling activity
136 over Modiolus modiolus reefs in the late 1990s was suspected of causing damage to
137 highly diverse biotopes in the north of the Lough (NIOA 2015). As a result the local
138 Government introduced a closed fishing zone in 2008 in an attempt to initiate natural
139 recovery (Roberts et al. 2011). The introduction of this closed zone increased the
140 activities of government enforcement officers and unintentionally the protection of the
141 small remaining resident O. edulis assemblages.
142 Owing to an examination of hydrodynamic regimens in the north of the Lough,
143 and recently reported increases in O. edulis densities (Smyth et al. 2009). It was
144 decided to investigate if there had been any evidence of unassisted high density stock
145 recovery. If verified the conditions under which recovery occurred could be examined
146 with the potential to provide test hypotheses for replication in future restoration
147 programmes. The criteria behind choosing the northern region of Strangford is based
148 on the presumption that established assemblages of oysters and increased policing of
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149 the marine environment would inadvertently lead to a rejuvenation and augmentation
150 of wild O. edulis stocks.
151
152 Materials and Methods
153 Study Area
154 Strangford Lough is located on the northeast coast of Northern Ireland and lies
155 between 54o 35’ N and 54o 20’ N and between 5o 41’ W and 5o 34’ W (Figure 1)
156 enclosing an area of 150 km2. The depth ranges from 14-60 m, with substrate varying
157 from bedrock to fine sediments (Kregting & Elsäβer 2014). The Lough can be divided
158 into northern and southern basins. The high retention hydrodynamic regimen in the
159 northern basin is particularly accommodating to larval pooling (Smyth et al. 2016). The
160 entrance to the southern basin is a long, narrow channel, known as The Narrows,
161 where current tidal velocity reaches ~3.5 m/s (Kregting & Elsäβer 2014).
162
163 Site Selection
164 Historical provenance, and recent oyster survey results (Day & McWilliams
165 1991; Smyth et al. 2009; Roberts et al. 2011; Guy et al. 2018) led to the northern basin
166 of Strangford Lough being selected as an area of possible undetected O. edulis bed
167 rejuvenation. Potential sites within the region had to meet habitat suitability
168 requirements as previously outlined in Kennedy and Roberts (1999) these included;
169 sufficient natural shell substrate to accommodate broad-scale settlement, an adequate
170 number of adult oysters for the conveyance of settlement cues and hydrodynamics
171 which would support larval retention. In studies over the preceding 12 years six sites
172 within the northern basin were identified as meeting these requirements to varying
173 degrees.
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174 The sites of Ballyreagh, Cunningburn and Greyabbey consistently produced
175 high density oyster settlements on a Mytilus edulis shell dominant substrate (Figures
176 2 to 5). Kircubbin, Pig Island and Ringhaddy where considered low density O. edulis
177 sites in comparison with a predominantly mud and shell fragment substrate (Kennedy
178 & Roberts 1999; Smyth et al. 2018). All sites were intertidal as extensive dive surveys
179 in the region between 2008 and 2011 had shown the subtidal substrate to consist of
180 heavy mud absent of a shell mix and therefore unsuitable for O. edulis larval settlement
181 (Roberts et al. 2011). The one exception was Ringhaddy a subtidal site mentioned in
182 the historical accounts of Lewis (1837). However, when examined in 2010 (Roberts et
183 al. 2011) any available hard substrate had succumbed to heavy siltation leaving
184 potential settlement surfaces in a poor state to accommodate high density larval
185 attachments, thus the site was sampled along the intertidal only.
186 All sites were located in the northern basin of the lough in close proximity to a
187 governmental Department of Agriculture sub-surface coastal monitoring buoy. The
188 recorded physical parameters which encompassed all waters within the survey sites
189 hydrodynamic regime included; water temperature of 2–17.6 °C, a mean salinity of 33,
190 mean nutrient concentrations (µmol l-1) of 2.8 ammonium, nitrate 13.5,
191 phosphorus 2, and silicate 4.3 and a mean nutrient load (ton year-1) of 1,202
192 nitrogen and 126 phosphorus (www.afbini.gov.uk/costal-monitoring).
193
194 Survey Techniques
195 Data collection from 2002-2014 were conducted as per those outlined in
196 Kennedy & Roberts (1999) the protocol was replicated again in 2018. Surveys were
197 undertaken in November during low spring tides of <0.5 m below chart datum. A
198 random belt transect and timed search methodology was employed with sampling
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199 taking place parallel to the low water mark within three 30 10m plots. Digital still
200 images were taken in-situ of gregarious settlement to record any O. edulis clusters (>2
201 oysters adhered together) known locally as ‘clocks’ (Figure 4). Oyster size was
202 recorded in-situ using a Vernier© caliper with measurements taken from the umbo to
203 the ventral front edge of the shell.
204 The influence of topographical variations on micro-hydrodynamics and O. edulis
205 larval settlement success has seldom been researched. During the 16-year survey
206 period, accumulations of conjoined oysters were recorded in high densities at sites
207 where high elevations of shell cultch dipped to form depressions within the shell
208 substrate. Therefore, a simple snap-shot topographical survey of site plots was
209 undertaken using a Nedo © F-series builders level and two York© ranging poles. This
210 allowed for the quantification of noticeable elevations and depressions of substrate
211 coverage from the horizontal plane (Figure 5 a-d). An area of >3m2 of elevation /
212 depression was required at sites to be considered for analysis.
213
214 Data Analysis
215 Multi-variate PERMANOVA of Bray-Curtis similarity matrices was used throughout
216 with 9999 permutations to determine the similarities of square root transformed data
217 of single and conjoined oyster settlements per; site, year, percent shell cover /m2,
218 harvesting protection and snapshot topographical features. The total area coverage
219 m2 of conjoined oysters per site and year was also examined using the same analytical
220 techniques. All statistical test were undertaken using PAST 3.25© (Hammer et al.
221 2001).
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223
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224 RESULTS
225 Single Settlement
226 The number of single settlements over the survey period was shown to be significantly
227 different between sites (F = 14.58, P = 0.0001). Pairwise post-hoc analysis (Table S1)
228 identified Ballyreagh, Kircubbin, Ringhaddy and Pig Island as significantly different (P
229 < 0.0005) from all sites. Differences in the number of single settlements at
230 Cunningburn and Greyabbey proved to be non-significant (P > 0.1). Differences in the
231 number of single O. edulis settlements per year over the survey period was shown not
232 to be significant (F = 1.72, P > 0.1).
233 The most northerly site of Ballyreagh produced the highest settlement densities
234 between 2002 and 2010 for single attachments over all five size cohorts (0-29, 30-59,
235 60-89, 90-119, 120-149 mm). However, settlements at Ballyreagh regressed rapidly
236 between 2014 and 2018. Cunningburn and Greyabbey proved to be the most prolific
237 single settlement sites post-2010 (Figure 2). Kircubbin, Pig Island and Ringhaddy
238 remained low density settlement sites throughout the survey period (Figure 2).
239
240 Multiple Attachment
241 The number of multiple attachments/clocks in relation to site during the survey period
242 was shown to be significant (F = 3.28, P < 0.005) (Figure 3). Pairwise post-hoc
243 analysis identified Cunningburn, Kircubbin, Ringhaddy and Pig Island as significantly
244 different (P < 0.05) (Table S2).
245 A significant difference (F = 2.08, P < 0.05) was detected in the number of multiple
246 attachments/clocks in relation to year, post-hoc analysis identified 2018 as the
247 survey year which was significantly different (P < 0.05) (Table S3).
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248 The total area of coverage in m2 attributed to conjoined oyster attachment was shown
249 to be significantly different (F = 1.58, P < 0.005) between sites. Post-hoc analysis
250 revealed Cunningburn, Kircubbin, Ringhaddy and Pig Island to be significantly
251 different (P < 0.05) in area m2 of conjoined settlement (Table S4). Analysis of area /m2
252 of conjoined oyster settlement and year proved not to be significant (F = 1.08, P =
253 0.3631).
254
255 Percentage of Shell Coverage
256 The percentage of available shell substrate within a site has been recognised by
257 numerous researchers as an influencing factor in the settlement success of O. edulis
258 (Bayne 1969; Kennedy & Roberts 1999; Christianen et al. 2018). Analysis revealed a
259 highly significant difference (F = 5.296, P = 0.0001) between the total percentage of
260 shell cover (no differentiation was made between shell types) per site and the total
261 density of annual oyster settlement. A pairwise post-hoc identified Kircubbin,
262 Ringhaddy and Pig Island as being significantly different (P <0.05) (Table S5).
263
264 Site Protection from Harvesting
265 Active site protection of commercial molluscan assemblages is a proven management
266 measure which can deter unregulated harvesting (Crawford et al. 2010). During the
267 surveys Cunningburn had an assemblage of O. edulis within a protected site. Site
268 protection and settlement densities per site revealed a significant difference (F =
269 4.041, P = 0.012).
270
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271 Density of Fecund Oysters (>60-150mm) in Relation to Total Density
272 The average total density per site of oysters considered fecund (>60mm/year 2, based
273 on Walne1964) was compared in relation to total overall density per site and year no
274 significant difference was detected (F= 8.066, P= 0.061).
275
276 Substrate Topography
277 The survey identified four sites with topographical height variations from the horizontal
278 plane of > 3m2 in area: Cunningburn 68-72mm, Ballyreagh 27-32mm, Pig Island
279 10mm, Kircubbin 10-14mm. No variations in shell height from the horizontal plane
280 were detected at Greyabbey and Ringhaddy. A significant difference (F= 3.029, P=
281 0.0003) was detected in oyster clump/clock density in relation to topographical height.
282 Post-hoc analysis showed Cunningburn to be significantly different (P <0.05) from the
283 remaining five sites and Pig Island significantly different (P <0.05) from Greyabbey
284 and Ringhaddy (Table S6).
285
286 Discussion
287 At Strangford Lough the site of Cunningburn was identified as accommodating
288 the most gregarious settlements over the 16 year survey period. The most prolific
289 solitary and clumped O. edulis settlement areas were all located on substrate
290 complexes dominated by shell. The lowest oyster densities were at sites where the
291 predominant substrate coverage was mixed mud. The most northerly site of
292 Ballyreagh showed high density settlements pre-2010 but experienced a dramatic
293 decline post-2006 particularly within the 30-59 mm size cohort. O. edulis densities
294 continued to decline at Ballyreagh throughout the survey period. With the site
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295 eventually becoming the least populated of the six by 2018. The three low density
296 sites, Ringhaddy, Kircubbin and Pig Island remained relatively static in regards to O.
297 edulis settlements throughout the 16 year period.
298 One of the most striking changes in the Strangford Lough oyster population was
299 the rapid density decline observed at Ballyreagh post-2006. Prior to 2002 (Nunn 1994;
300 Kennedy & Roberts 1999) no historical accounts of O. edulis settlements existed for
301 Ballyreagh. However, by 2004 an estimated population of >300,000 O. edulis had
302 settled in densities of >30 m2 (Smyth 2009) although by 2018 <20 individuals
303 remained. Pathogen or pollution induced mortalities can be disregarded as an
304 explanation for population decline as no empty oyster valves were recorded and shell
305 debris would have lingered within the low-velocity, low–flush regimen. Numerous
306 witnessed reports from members of the general public of shellfish gatherers in the
307 vicinity of Ballyreagh between 2004 and 2006 suggest that sporadic subsistence and
308 commercial harvesting was the overriding influencer in population declines (Smyth et
309 al. 2009).
310 Oyster densities at the remaining five sites fluctuated over the 16 years though
311 not to the extent experienced at Ballyreagh this may have been because of an increase
312 in policing. However, it would be assumptive to attribute the maintenance of oyster
313 densities to policing alone. It may be simply that stocks had become non-viable for
314 harvesting due to the low Catch Per Unit Effort (CPUE). Similar harvesting scenarios
315 have been described for other intertidally accessible species; Amiantis purpurata,
316 Cymbula granatina, Lucina pectinata, Panopea abrupta, Perna perno (Kyle et al. 1997;
317 Tomalin et al. 1998; Rondinelli & Barros, 2010). Continuous low-level subsistence
318 gathering of at sites may be impeding recovery and keeping standing stocks stagnant.
319 Monthly observations of accessible assemblages of market sized oysters would assist
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320 in the monitoring of shellfish gathering and give a better understanding to the
321 population dynamics of native oysters within Strangford.
322 A further detrimental effect of harvesting pressure on mature oysters is the
323 fragmentation of fecund standing stock (Rondinelli & Barros 2010). This can result in
324 a compromised Allee effect and a decrease in successful spawns. Eventually leaving
325 population dynamics inert and as natural mortality ensues the species eventually
326 becomes reproductively non-functional (Marshall et al. 2003; Turra et al. 2016). Guy
327 et al. (2018) showed that O. edulis is particularly susceptible to this chain of events,
328 as a nearest neighbour of < 1.5 m brooded significantly more larvae than those with a
329 nearest neighbour of > 1.5 m. The findings at the low-density sites and the heavily
330 harvested site of Ballyreagh concur with Guy et al. (2018). As adult oysters were
331 removed from the population post-2006 recruitment slowed significantly with the
332 Ballyreagh stock virtually non-existent by 2018.
333 During the research a significant increase in the gregarious nature of larval
334 settlement at Cunningburn was noticed. The site produced settlement complexes of >
335 16 conjoined oysters and a total area coverage of clumps within the survey plots of
336 6.8 m2. This was unique among survey sites and represents the first documented
337 occurrence of conjoined O. edulis settlements in this density in Ireland. Cunningburn
338 had site properties similar to both Ballyreagh and Greyabbey however the volume of
339 post-2014 oyster clump settlements suggested site specific properties had influenced
340 the attachments. A comparison between sites identified Cunningburn as possessing
341 some distinctive characteristics which may have influenced the gregarious behaviour
342 most notably; topographical shell formations, % shell substrate coverage, number of
343 in-situ fecund adults and protection from harvesting.
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344 The topographical nature of the shell substrate accumulations at Cunningburn
345 were markedly different from the other sites. Although shell coverage /m2 was similar
346 at Greyabbey and Ballyreagh the M. edulis concentrations at Cunningburn formed
347 undulating banks which created a network of large intertidal pools. These pools held
348 the majority of oysters found at the site and appeared to have acted as natural spatting
349 ponds. It is possible that the formations provided a containment area for larvae to
350 concentrate in high densities thereby increasing the potential for focused gregarious
351 settlement within these Cunningburn pools, which would have several advantages to
352 reduce mortality. The ponds would provide protection against; air exposure over tidal
353 cycles, low winter temperatures and visual detection from harvesters.
354 The use of natural spatting ponds or “polls” in oyster culture has been
355 considerable, with records dating as far back as A.D. 43. when Romans stocked
356 naturally occurring pools in Northern France to act as primitive mariculture systems
357 (Horváth et al. 2012). Historically, the spatting pond was the stock enhancement
358 technique of choice in many regions of Europe (Hedgecock & Davis 2007). However,
359 concerns regarding the genetic fitness of the progeny, high density disease transfer
360 and the development of improved hatchery culture led to their demise (Lallias et al.
361 2010). The intertidal pool structure and high-density settlements discovered during this
362 study present a hypothesis worthy of testing for future native oyster
363 rejuvenation/reintroduction programmes. If a section within a restoration cultch lay was
364 formed into an undulating bank of shell it could provide the micro hydro-dynamics
365 suitable to replicate the larval settlement at Cunningburn.
366 The availability of shell, as opposed to shell type, has been shown to be
367 influential in settlement success (Smyth et al. 2018). A significant higher density of O.
368 edulis attachments were discovered at Cunningburn post-2014 when compared to
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369 other sites. In contrast to the findings of Smyth et al. (2018) the survey showed that
370 when available, at Strangford Lough O. edulis pediveligers attachment material of
371 choice was the living edge of a live oyster. Researchers have emphasised this fact
372 previously in relation to larval settlements within Ostrediae spat (Breitburg et al. 2000;
373 Tamburri et al. 2008).
374 The high density of oysters >60mm at Cunningburn and their associated
375 conspecific chemical cues may have also had an influence on settlement behaviour
376 (Rodriguez et al. 2019). An overview of the three hypotheses related to O. edulis and
377 adult density related chemical cues can help explain. The first indicates conspecifics
378 as the source therefore a high-density mature population is required (Keck et al. 1971).
379 The second suggests the importance of biofilms on oyster shells, therefore high
380 density of shell material is required (Bonar et al. 1990). The third identifies high
381 densities of both live oysters and biofilms on shell, as producing settlement inducing
382 cues which act synergistically (Tamburri et al. 2008). The O. edulis aquaculture and
383 mariculture sector concurs with the hypothesis of high densities of conspecifics as an
384 explanation for increased oyster settlements (Hugh-Jones 2003; Galley et al. 2017).
385 Oyster growers have long considered live and dead oyster valves as the most effective
386 settlement surfaces (Yamaguchi 1994). At the Loch Ryan O. edullis fishery in
387 Scotland, >100 spat have been recorded on a single live oyster (Hugh-Jones 2003).
388 In Ireland, at the Bertraghboy fishery, >80 spat have been recorded regularly on wild
389 O. edulis (Barry 1981). There are similar reports from aquaculturists throughout
390 Europe of high density spat attachments on living O. edulis within hatcheries
391 (Drinkwaard 1998; Culloty & Mulcahy, 2007). The findings of this present research are
392 certainly worthy of further investigation as the densities of live adult O. edulis may be
393 an important factor when attempting to establish gregarious settlement events.
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394 The active protection from illicit harvesting at Cunningburn was considered as
395 a dominant influence. The location of the O. edulis population is in close proximity to
396 a private yacht club where trespassers onto the adjacent foreshore are actively
397 challenged by club members. This acts as a powerful deterrent. Nevertheless, as wild
398 stocks at other unrestricted sites decline and CPUE decrease, the concentrated
399 assemblages at Cunningburn will become an attractive proposition worthy of trespass
400 for unscrupulous harvesters. Unregulated harvesting events such as those described
401 at Ballyreagh where, 300,000 individuals were removed, can have a devastating
402 impact on a conservation project (Bostock et al. 2010; Guy et al. 2018). Presently
403 throughout Europe a significant amount of time, effort and finance have been
404 committed to restoring O. edulis to a self-sustaining status (Helmer et al. 2019; Pogoda
405 et al. 2019). It is vital that NGO’s, Habitat Managers and Governments recognise the
406 detrimental consequences of mass removal events and produce preventative
407 measures to counter such actions.
408 Historical European native oyster regions, experience a suite of hindrances in
409 regards to recruitment and reintroduction; a lack of effective larval density, water
410 quality, disease, anthropogenic disturbance and substrate availability (Laing et al.
411 2006). The observations described during this survey have highlighted a number of
412 aspects of O. edulis settlement dynamics which are not fully understood and a
413 considerable knowledge gap exists which therefore warrant trial when investigating
414 restorative gregarious, O. edulis settlements.
415 It may be, that historical accounts such as those described by Orton (1937)
416 which refer to the North Sea grounds as; “being built of oysters, knitted and interlaced
417 with countless other invertebrates with the bottom hardened as a living crust”
418 (Houziaux et al. 2008) are beyond the capabilities of present restoration initiatives.
17
Ostrea edulis unassisted restoration
419 However, the tentative high-density bed settlements and the number of clumped
420 oysters recorded during this research should be considered inspirational to all those
421 involved in the re-establishment of Ostrea edulis. As the task which was once
422 considered almost unachievable has now been revealed as possibly attainable.
423
424
425
426 Acknowledgements: The authors would like to thank the following funding bodies for
427 making this work possible: EPSRC Engineering and Physical Sciences Research
428 Council, the Marine Institute Ireland, the Department for the Economy Northern
429 Ireland, the Bryden Centre, the Departments of Employment and Learning, and
430 Agriculture and Rural Development (EU Building Sustainable Development
431 Programme) Northern Ireland.
432
433
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603
604
605
606
607
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611
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613
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614 FIGURES
615 Figure 1. Strangford Lough and the six survey sites with substrate constitution at
616 sample plots.
617
618 Figure 2. Individual Ostrea edulis density per size cohort at sites between 2002 and 619 2018. (Site codes are: C- Cunningburn, B- Ballyreagh, G- Greyabbey, K- Kircubbin, R-Ringhaddy, P- Pig Island).
620
621 Figure 3. Total area m2 of multiple attachment Ostrea edulis settlement per site and
622 year.
623
624 Figure 4. Ostrea edulis clumps/clocks at intertidal pools Cunningburn
625
626 Figure 5. Lateral cross-section schematics and in-situ image of undulating mussel 627 bank (Mytilus edulis) formations at Cunningburn site.
628
629
26
Ostrea edulis unassisted restoration
630
631 Figure 1. Strangford Lough and the six survey sites with substrate constitution at
632 sample plots.
633
634
27
Ostrea edulis unassisted restoration
635
636
Ostrea edulis Size Cohorts 2002-2018 180
160 0-29 mm 140 30-59 mm 120 60-89 mm 100 90-119 mm
80 120-149 mm
60
Number single of attachments 40
20
0
B/02 P/06 K/14 K/02 P/02 B/06 K/06 B/10 K/10 P/10 B/14 P/14 B/18 K/18 P/18
C/06 R/10 C/02 R/02 R/06 C/10 C/14 R/14 C/18 R/18
G/18 G/02 G/06 G/10 G/14
637 Site 638
639 Figure 2. Individual Ostrea edulis density per size cohort at sites between 2002 and 640 2018 (Site codes are: C- Cunningburn, B- Ballyreagh, G- Greyabbey, K- Kircubbin, 641 R-Ringhaddy, P- Pig Island).
642
643
644
645
28
Ostrea edulis unassisted restoration
7.5 7 6.5 6 5.5 5
2 4.5 4 3.5
Area Area m 3 2.5 2 1.5 1 0.5
0
C/14 B/02 G/02 C/02 K/02 R/02 P/02 B/06 G/06 C/06 K/06 R/06 P/06 B/10 G/10 C/10 K/10 R/10 P/10 B/14 G/14 K/14 R/14 P/14 B/18 G/18 C/18 K/18 R/18 P/18
646 Site 647
648 Figure 3. Total area m2 of multiple attachment Ostrea edulis settlement per site and
649 year.
650
651
652
653
654
655
656
657
658
659
660
661
29
Ostrea edulis unassisted restoration
662
663
664
665
666
667
668
669
670
671
672
673
674
675
676
677
678
679
680
681
682
683
684 Figure 4. Ostrea edulis clumps/clocks at intertidal pools Cunningburn
685
686
30
Ostrea edulis unassisted restoration
687
688
689
690
691
692 a. Movement of O. edulis veliger and pediveliger larvae during incoming high spring tide 693
694
695
696
697 b. 698 O. edulis veliger and pediveliger containment during the ebbing tide 699
700
701
702
703 c. 704 O. edulis veliger and pediveliger become more densely concentrated within the 705 intertidal mussel pools during the lowest ebb. The undulating mussel banks maintain this level of tidal retention throughout the tidal cycle. 706
707
708
709
710
711 d. Figure 5. Lateral cross-section schematics and in-situ image of an undulating mussel bank (Mytilus edulis) formation at Cunningburn. 31