Ecology and management of European biogenic reefs

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Biogenic reefs are compact structures formed by living organisms that provide habitat for other species. This article focuses on four important reef-forming taxa of European coastal and shelf waters: the tube-building polychaetes Sabellaria spinulosa and Sabellaria alveolata, and the mussels Mytilus spp. and Modiolus modiolus. It describes their environmental requirements, development and natural dynamics, vulnerability to natural and anthropogenic disturbance, recovery and management. Their European distribution and temporal variability are discussed in Biogenic reefs of Europe and temporal variability.


General features

Figure 1: Sponge forming part of a newly discovered cold water reef on Anthon Dohrn Seamount (copyright: JNCC)

The classic definition of a reef is a submerged structure rising from the surrounding seafloor that forms a hazard to shipping[1]. In recent years, this definition has undergone several transformations due to emerging exceptions to this rule (e.g. cold-water coral reefs[2]). Modern consensus now defines reefs as being any structure in the marine environment that arises from the seabed and covers an extensive area. Some management agencies have expanded their interpretation of reef to include both, geogenic formations of bedrock, cobbles or boulders and biogenic concretions created by structure-forming coral, bivalve and polychaete species. Reefs vary in size and structure, and the communities they support depend strongly on their location and composition. In the waters around Europe, several key organisms form biogenic reefs. These can range from enormous structures formed by cold-water coral species such as Lophelia pertusa[3] (Figure 1), to smaller aggregations of tube-building polychaete worms such as Sabellaria spinulosa[4]. Reefs formed by scleractinian cold-water corals such as Lophelia pertusa occur at great water depths, typically between 200-1000 m.

Species and Characteristics

This section describes reefs formed by S. spinulosa, aggregations of the bivalve Mytilus spp., the polychaetes Sabellaria alveolata, Serpula vermicularis and Ficopomatus enigmaticus. See also the article Biogenic reefs of Europe and temporal variability.

Sabellaria spinulosa

In contrast to S. alveolata, the closely related Sabellaria spinulosa is typically recorded subtidally and only rarely in intertidal habitat[5]. Individuals commonly occur alone or in small aggregations. Under favourable conditions, they form thin layers or larger reefs reaching approximately 30 cm in height[6]. The tubes are made of sediment similar to that used by S. alveolata, but are thinner and more upright. The sedimentary composition of tubes show similarities with, but morphologically are much thinner and upright. The tubes, whilst fragile, are deceptively strong and are formed by several layers of sediment ranging from large particles on the exterior to smaller particles on the interior with a parchment-like interior tube.

Sabellaria alveolata

Figure 2. The 'Récif Les Hermelles', reef built by Sabellaria alveolata in the Baie du Mont Saint Michel, France.

Sabellaria alveolata is a sedentary tube-dwelling polychaete that constructs tubes from suspended sediment and shell fragments[7]. Although S. alveolata does occasionally occur as individuals, it is more commonly found in colonies. Colonies occur mainly as two forms: veneers that adhere closely to rocks in the mid-intertidal zone, and reefs that develop mainly in the lower intertidal zone. Veneers can reach 30 cm in height; reefs can reach 1.5 m and extend across large areas of sandflat[7]. Reefs, which are generally found at the lower level of the intertidal zone, are up to 1.5 m in height and can develop to cover acres of sand flats[8]. This species is typically located on exposed, open coasts with reasonable to substantial water movement[9]. It is predominantly intertidal, but has been observed subtidally on rare occasions (e.g. the Severn Estuary[10], off the Cumbrian coast[11]). In dense aggregations, the tubes form a characteristic honeycomb structure. Each tube is narrow at its base and widens towards its entrance. This structure is easily damaged, and undergoes almost continual repair by living worms[7]. The records of Sabellaria alveolata throughout Europe are greater in northern latitudes. This is an obvious artefact of data reporting to OBIS as S. alveolata has been reported to be widely distributed in the France, Spain and Portugal and extends as far south as Morocco[8][9]. This species builds the largest reefs on the European coast; in particular the “Les Hermelles” reef in the Baie du Mont Saint Michel in France is over 100 hectares (Figure 2) and is considered the largest reef in Europe[8][12].

Serpula vermicularis

Figure 3. Cold-water reef made of the tubes from the worm Serpula vermicularis.

The serpulid worm Serpula vermicularis builds calcareous tubes that can be 4-5 mm in diametre and 150 mm in length (Figure 3). The tubes are occasionally ringed and cylindrical in form, with lengthwise ridges. This species is usually solitary, but aggregations that can be classed as reefs have been recorded at sheltered locations on the west coast of Scotland[13][14]. Their tubes are attached to hard substrata, subtidally to depths of a maximum of 250 m. Reefs formed by this species are particularly rare and occur only in well-sheltered sea lochs with limited currents and wave exposure.

Ficopomatus enigmaticus

This polychaete tubeworm of the Serpulidae family is native of subtropical Australia, but has invaded sheltered brackish water systems worldwide, including regions with lower temperatures, for example northern Europe (e.g. Baltic Sea)[15]. F. enigmaticus is a filter feeder, feeding on suspended detritus and phytoplankton. It colonizes stable substrate or hard surfaces, but it also occurs on soft sediment. F. enigmaticus is frequently found in ports and marinas or lagoons with man-made embankments[16]. It is an eco-engineer, building reefs that consist of clumps of vertical tubes (up to 180,000 per m2) which are cemented together. These reefs act as sediment traps, facilitating particles’ deposition and accumulation. They can take various shapes: hemispherical reefs, fringing reefs along rocky shorelines or circular reefs, all of modest size (generally less than 10 m). The tubeworms release faeces and pseudofaeces that enrich the sediment with organic carbon and nitrogen compounds. The reefs provide shelter and food for many biota, such as crabs, gastropods, amphipods, and polychaetes[17]. Reef-associated communities often include non-indigenous species[18].

Mytilus spp.

Figure 4. Mussel bed reef.

Mytilus edulis and Mytilus galloprovincialis co-occur throughout much of Europe. Despite being two distinct species, they are difficult to identify in the field and are known to hybridize. In this article, both species are referred to collectively as Mytilus spp. Aggregations of Mytilus spp. occur in shallow subtidal waters along much of the European coast. This species has a major reef-forming role (Figure 4), as Mytilus spp. can form bioconstructions that range in size from small clumps to beds of several hectares[19]. Individuals of this species are usually semi-infaunal, projecting above the sediment, creating an irregular surface topography[20]. This surface complexity alters water movement over the bottom, producing boundary layer flow regimes that affect the delivery and resuspension of sediment particles in mussel beds[21][22][23][24]. In addition to structuring the hydrodynamic environment, Mytilus spp. also modify their surroundings by filtering suspended particles and depositing faeces and pseudofaeces[25][26]. The heterogeneous topography generated by the mussels also consolidate and entrain sediments[22][27].

Processes and mechanisms driving natural dynamics & ecosystem development

Biogenic reefs are compact structures formed through the activities of living organisms. Their structure and size vary, as do the communities they support. They do not share an uniform structure and vary in spatial scale. Moreover, the life they support is greatly dependent upon location and composition. Dense colonies of several species are widely considered to be reef in Europe (see Biogenic reefs of Europe and temporal variability). This section focuses on four reef-forming taxa that can influence sediment retention, bed stability and wave attenuation: Sabellaria spinulosa, Sabellaria alveolata, Mytilus spp. and Modiolus modiolus. In this section, the processes and mechanisms driving natural dynamics and ecosystem development of biogenic reefs are discussed for each group in turn.

Sabellaria spinulosa

Environmental Requirements
S. spinulosa (or Ross worm) is thought to require stable foundations on which to settle and establish a tube[28][29][30] and is thus likely to favour substrata which include bedrock; boulders, cobbles, mixed substrata; and mixed sediment[31]. Although it is assumed that a firm substratum is required for colony establishment, it has been suggested that a reef can increase in extent without the need for hard substratum[32]. Many studies have reported extensive colonies in predominantly sandy areas[33][34][35][36]). Observations from The Wash, England show that S. spinulosa had ‘seeded’ on shell fragments predominantly from blue or horse mussels. Observations on the Dutch Continental Shelf also show that patchy S. spinulosa reefs can persist in dynamic sandy-bottom environments and support substantially greater epifaunal density and species richness than surrounding sandy habitat[37]. As S. spinulosa is a sedentary species, it relies on wave and current action to supply food and wash away waste products[38]. Strong water movement is required for food provisions, but is perhaps more important to raise sediment into suspension for tube building[39]. As a result, S. spinulosa colonies are typically located in areas of weak to moderately strong water flow[40]. It also appears to favour locations around the edges of sand banks or areas with sand waves[41]. A habitat-suitability analysis for the Wadden Sea identified water depth, current velocity, salinity, sediment grain size and availability of settlement substrate as important controls on S. spinulosa occurrence[42][43]. S. spinulosa typically occurs subtidally in depths of a few metres to up to 40 m depth[44][45][31][46], but can occur in depths up to 600 m. S. spinulosa occasionally occurs in the lower intertidal zone[46].
Reproduction and Development
The fecundity and recruitment of S. spinulosa is known to be variable[47][48][49][45]. The family Sabellariidae are broadcast spawners, reproducing sexually, resulting in larvae that drift passively in the plankton[34][50]. The larvae can spend a few weeks to several months in the plankton[51] before seeking appropriate conditions for settlement[52][50]. If conditions are unsuitable, the larvae are able to delay metamorphosis for several weeks. Physical factors alone have limited influence on settlement[52] and settlement and metamorphosis is strongly influenced by the tube cement of other sabellariids[52]1970[53][50][54]. This mechanism ensures settlement in a suitable habitat and promotes the development of large colonies. Despite only a few studies investigating the rate at which S. spinulosa can extend their dwelling tubes[55][56] being exceptions), it appears that sabellariid reefs develop quickly following successful settlement[47][57][58][59]. Observations show that tube extension rates are highly variable and that they could grow up to 6 mm a day for several days when provided with an adequate sediment supply[60]. Little is known about the longevity of S. spinulosa colonies, but sabellariids are expected to survive for 1-2 years[61][62][63], with some reports of longer life spans[64][45]. It is likely that the age of an actual colony may greatly exceed the age of the oldest individuals. This is particularly likely as sabellariid larvae are stimulated to metamorphose by conspecific secretions, encouraging continuous succession of generations.

Sabellaria alveolata

Environmental Requirements

Figure 5: Images illustrating the various stages of development of S.alveolata reef at Bude, Cornwall (photos L. Firth).

S. alveolata (or honeycomb worm) generally requires hard substrata on which to develop, but these must be in areas with a good supply of suspended coarse sediment for tube building. S. alveolata reefs are known to form on a range of substrata from pebble to bedrock[65]. Reefs therefore commonly form on bodies of rock or boulders surrounded by sand. Observations show that settlement of S. alveolata can be facilitated by the sand mason Lanice conchilega which can stabilize sand well enough to allow colonization by S. alveolata[66]. Settlement occurs mainly on existing colonies or their dead remains (Figure 5). Water movement of sufficient intensity is a prime requirement to suspend coarse sand particles, thus making them available for the building of worm tubes. In many British localities such as the south west of England, much of Wales and the Cumbrian coast, the former seem more important. In other areas, such as parts of the Severn Estuary, tidal suspension is probably very important. However, S. alveolata is generally absent in very exposed peninsulas such as the Lleyn, Pembrokeshire and the extreme south west of Cornwall, which probably relates to the effect of water movement on [[[recruitment]][65]. Habitat-suitability modelling further indicates that the distribution of S. alveolata depends on interacting environmental factors and cannot be explained by temperature alone[67].
Reproduction and Development
It is thought that the larvae of S. alveolata spend 6 weeks to 6 months in the plankton[52][48] allowing widespread dispersal. According to observations in the British Isles, slight settlement occurs every month except in July, but in 14 years of monitoring (1961 to 1975) [68] only three heavy settlements (1966, 1970 and 1975) occurred from September to November or December. Subsequent studies have revealed that the intensity of settlement is extremely variable, both temporally and spatially[69][65]. Settlement occurs mainly on existing colonies or their dead remains; chemical stimulation seems to be involved, and this can come from S. spinulosa tubes as well as from S. alveolata[48][69][65].

Ficopomatus enigmaticus

This polychaete tubeworm of the Serpulidae family is native of subtropical Australia, but has invaded sheltered brackish water systems worldwide, including regions with lower temperatures, for example northern Europe (e.g. Baltic Sea)[70]. F. enigmaticus is a filter feeder, feeding on suspended detritus and phytoplankton. It colonizes stable substrate or hard surfaces, but it also occurs on soft sediment. F. enigmaticus is frequently found in ports and marinas or lagoons with man-made embankments[71]. It is an eco-engineer, building reefs that consist of clumps of vertical tubes (up to 180,000 per m2) which are cemented together. These reefs act as sediment traps, facilitating particles’ deposition and accumulation. They can take various shapes: hemispherical reefs, fringing reefs along rocky shorelines or circular reefs, all of modest size (generally less than 10 m). The tubeworms release faeces and pseudofaeces that enrich the sediment with organic carbon and nitrogen compounds. The reefs provide shelter and food for many biota, such as crabs, gastropods, amphipods, and polychaetes[72]. Reef-associated communities often include non-indigenous species[73].

Mytilus spp.

Environmental Requirements
The widespread distribution of the M. edulis is a reflection of its tolerance of a wide range of environmental conditions. Natural reefs typically occur on firm, mixed sediments in relatively wave-sheltered estuaries and bays characterized by strong currents[74]. In more exposed areas, larger colonies are only able to develop on hard and stable substrata such as rock or large boulders[75]. Conversely, in sheltered environments large beds may develop on more sandy substrates[76]. Mussels produce byssal threads which anchor them to the substratum and each other, enabling large beds to develop. Mussels can grow in all but the most exposed conditions where their byssus threads can provide anchorage against wave action and water flow. As M. edulis is a sessile filter feeder, it requires sufficient water to flow to bring food and wash away waste. Larger beds require higher flow in order to provide sufficient food supply to high numbers of individuals. It is generally considered that this water movement is best provided by tidal currents rather than wave action, though the latter may also contribute in some areas[74]. M. edulis is tolerant of a wide range of salinities, being found in locations ranging from estuarine to fully marine, but larger reefs typically occur within the lower third of the intertidal and in the mid to lower reaches of the estuary[74]. M. edulis reefs do form subtidally and have been reported to occur at depths of 30 m. The upper limits of M. edulis are thought to be set by temperature and desiccations stress[77] in addition to reduced feeding[78]. The lower limits are generally set by biological factors such as competition and predation with physical factors playing a secondary role[74].
Reproduction and Development
The M. edulis fecundity and recruitment success is highly variable, both temporally and spatially. It can reproduce in its first year and can spawn throughout the year, with a major spawning event usually occurring in the spring[75]. Larvae can survive in the plankton for 2‐4 weeks before metamorphosis, although this can be up to 6 months, depending on availability of food, suitable substrate and temperature[74]. Settlement can be either a one-stage or a two‐stage process. Some larvae settle directly on adult beds[79] or they can temporarily settle onto sublittoral filamentous substrata such as algae or hydroids before becoming detached, and eventually settling onto an adult bed[80]. It is thought that this may be a mechanism for reducing competition between very young and adult mussels, and/or to prevent filtration of the larvae by the adult mussels. High densities of settling spat have been reported in Ireland[79], but more commonly modest recruitment between the shells of adult mussels provides sufficient supply to maintain persistent beds[74]. Conversely, heavy recruitment may not necessarily lead to the formation or maintenance of a dense bed or reef if predation or losses due to wave action are high. M. edulis growth and production can be extremely high, particularly in sheltered or estuarine areas. It has been reported that M. edulis accounts for 20% of the total macrobenthic production in the Wadden Sea[81], whilst the production by two year classes was estimated to be 2.5‐3 times their maximum standing crop, with few mussels surviving beyond their third year[82]. It is thought that the majority of mussels do not survive beyond 3 years of age[83], but there are reports of individuals surviving beyond 15 years[84].

Modiolus modiolus

Environmental Requirements
Despite typically occurring on hard substrata, M. modiolus (or horse mussel) beds and reefs are capable of forming on a variety of sedimentary bottoms, ranging from muddy substrata in some sea lochs to quite coarse mixed sediments containing many stones and shells. Larvae can also settle on artificial substrates such as oil rigs and can form reefs on these structures. The byssus threads of adult M. modiolus provide a suitable substrate for attachment and protection from predators. Beds occurring infaunally can lack available byssus threads and thus limit recruitment[85] and the development of larger beds. M. modiolus has a very wide depth distribution, typically being found subtidally from a few metres of depth right down to depths of 280 m[86]. Intertidal populations have occasionally been reported[87], but these are thought to be limited by temperature and desiccation stress associated with aerial exposure[88][87]. The densest populations, which are regarded as reefs, are found between 5 and 50 m in British waters[74], whilst infaunal reefs have been found at over 80 m in the Bay of Fundy[89].
Reproduction and Development
M. modiolus is a long-lived species with individuals only reaching sexual maturity between 3 and 6 years of age. It is thought that this adaptation is a response to high predation on juvenile mussels, thereby channeling energetic resources towards growth in early life. As a result, M. modiolus exhibits rapid growth in the first few years of life, followed by much slower growth following sexual maturation[90]. M. modiolus spawning is known to be variable, both temporally and spatially. In Strangford Lough, Northern Ireland, slight spawning is known to occur year-round, with no apparent peak[91][92]. Conversely, in Scandinavia, a spawning peak occurs in June, followed by a period of gonad redevelopment. Spawning is temperature dependent and is reported to occur within a narrow temperature range (7-10 °C). It is thought that the relatively constant temperatures in Strangford Lough facilitate the year-round spawning[92]. M. modiolus in the Irish Sea off the SE coast of the Isle of Man has been observed to follow an annual cycle of gonad development with a peak occurring in spring/summer, with trickle spawning occurring all year round[93].

Ecosystem services

Performance and sensitivity

Biogenic reef builders (including mussel beds and worm reefs) have recently been named ”bioconstructors”[94]. They can be defined as organisms that build films, crusts, mounds or reefs of material that they either produce internally (e.g., biogenic carbonate deposition), bind from other sources (using organic cement e.g. worm reefs) or develop from a combination of the two (e.g. mussel beds). The majority of research on biogenic reefs has focused on the morphology of the structures and their function in enhancing biodiversity by habitat creation[95][96]. Few studies have focused specifically on the geomorphological contributions of bioconstructions themselves, particularly in relation to their potential roles in natural coastal defence. Hence, there is much need for research on natural reefs both in terms of their intrinsic functions such as growth, development, resistance and resilience as well as their importance in larger-scale ecosystem functioning which may benefit developing predictive models of biocomplex responses to predicted sea-level rise and global climate change.

Figure 6. Seabed colonized by the worm Sabellaria spinulosa.

Sabellaria spinulosa

Sabellaria spinulosa (Figure 6) usually occurs subtidally in areas of high water flow, and is relatively tolerant of wave and tidal forcing. However, it has been suggested that an increase in wave or tidal flow may reduce the stability of the attachment substratum resulting in increased scouring and mortality of individuals[97]. It is a relatively disturbance-tolerant pioneer species[97]. Fisheries for the pink shrimp Pandalus montagui and brown shrimps Crangon crangon have been implicated in the loss or damage of reefs but experimental and observational studies have indicated only minor damage to tubes and rapid recovery as a result of shrimp fisheries. Nevertheless, populations, especially if as loose aggregations, may be displaced by mobile fishing gear. In gregarious aggregations, Sabellaria spinulosa tubes intertwine to form a rigid structure that collects sand, detritus, and fecal material between the tubes[98]. In reefs, the bound sediment comprising the S. spinulosa tubes typically smothers the underlying substrate. In contrast, the consolidated tubes of crustose colonies typically form a thin veneer across the surface of the underlying substratum and do not necessarily cement larger pebbles together. Their ability to trap sediment is less and this growth form is considered to be more susceptible to fragmentation during winter storms for instance and to damage from physical impacts than a more upright morphology[4]. It was observed that S. spinulosa consistently utilised a lower mean particle size than that of the background sediment when provided with well-sorted medium sands[99]. Under sediment-starved conditions, there was net erosion of colonies whereas under intermediate and high sediment rates there was consistent cumulative growth. This means S. spinulosa requires water to be relatively turbid (i.e. high flow periods and storm events) in order for the tubes to grow.

Figure 7. Reef structure of cemented coarse sand consisting of tubes produced by the worm Sabellaria alveolata.

Sabellaria alveolata

Sabellaria alveolata (Figure 7) constructs tubes from sand-sized mineral grains and shell debris, referentially sorting sand grains and accumulating heavy minerals[100][101][102]. S. alveolata is widely distributed throughout Europe. It forms veneers and reefs. Reefs are generally found at the lower level of the intertidal zone[8] and may perform indirect and direct bioprotectional roles. Their structures might influence local hydrodynamics or energy regimes, and preferentially store sediment that would otherwise be 'loose' in the system, available to physically abrade shore platforms[103][104]. Sabellaria reefs affect both biodiversity and biogeochemical processes[105]. Sabellaria alveolata is typically threatened by the physical disturbance of removal from tubes and substratum loss. It has been suggested that most colonies die through eventual break up by wave action[97]. Increased exposure will potentially result in shorter colony lives. S. alveolata is a southern species and is at the northern end of its range in Britain. It has been shown to be severely affected by low winter temperatures[106]. Despite the current trends in global warming, winter 2009/2010 was the coldest on record in Europe, which may have negatively affected S. alveolata at its range edges. Continued monitoring is necessary to detect future changes.

S. vermicularis

S. vermicularis is a subtidal species found permanently attached to the substratum. It is relatively intolerant to strong increased water flow rates and strong wave action which interfere with its feeding. If strong wave action occurs over prolonged periods of time, death can occur. S. vermicularis forms reefs in sheltered areas (e.g. sea lochs) where it is likely to be even more intolerant to wave action.

Mytilus spp.

Large aggregations of Mytilus spp. are found in shallow marine environments along much of the European coast of Europe. Mytilus spp. is a major bioconstructor, forming rough and sediment retaining mussel patches that range in size from small clumps to large beds of several hectares[19]. Mytilus spp. also modify their environment through active filtration and the subsequent formation of biodeposits of seston[25]. Mussels could be used to reduce turbidity by biofiltration[107], which may benefit the reintroduction of sea grasses[108]. The beds can dissipate wave energy, thereby protecting salt marshes from erosion[109]. Extra deposition of fine sediments in these areas by a reduction of flow velocities or fixation as (pseudo-) fecal matter is also thought to increase the resilience of salt marshes. Mytilus spp. is semi-infaunal. Projecting above the sediment, individuals create an irregular surface topography that produces a boundary layer flow over the bottom that affects the delivery and resuspension of sediment particles in mussel beds[22][23]. A process-based model of the interaction between a young mussel bed and fine sediment[110] showed that a combination of active deposition via filtration and reduction in flow velocity due to increased roughness leads to high net deposition in the mussel bed. In addition, young mussels can quickly climb on top of deposited material resulting in rapid trapping of large amounts of fine sediment. In the wake of the mussel bed, deposition is also high because of reduced flow velocities. Repeated substratum loss and recruitment results in a patchy distribution of mussels on the shore[111]. Storms and tidal surges are known to destroy mussel beds, often over hundreds of hectares in the Wash, Morecambe Bay and the Wadden Sea. Feasibility of using the biogeomorphological impact of mussel beds for ecological engineering purposes[112] requires further investigation.

Modiolus modiolus

Modiolus modiolus reefs provide structurally complex habitat that supports diverse associated benthic communities. A survey of 16 M. modiolus reefs across the northeast Atlantic recorded high species richness and showed that the associated communities differed substantially among reefs, indicating that conservation of multiple reef sites is important for maintaining regional biodiversity[113].

Vulnerability & threats

General summary

This section is divided up into (1) the vulnerability and (2) the threats (biological, chemical and physical) to each species in turn: Sabellaria spinulosa; Sabellaria alveolata; Mytilus spp. and Modiolus modiolus. In this section, we refer to the sensitivity, vulnerability and potential for recovery of the habitat to sea-level rise and storm events. In the case of natural reefs, flooding is not applicable and is therefore not discussed here. Much of the information from this section was sourced from (the Marine Life Information Network website). We have adopted the terminology used by MarLIN with definitions below. In the following sections, we have identified the factors that are most likely to be associated with sea-level rise and storm events for each species. The ‘intolerance’, ‘sensitivity’ and ‘recoverability’ of each species are presented in table format.
Intolerance is the susceptibility of a habitat, community or species (i.e. the components of a biotope) to damage, or death, from an external factor. Intolerance must be assessed relative to change in a specific factor.
Recoverability is the ability of a habitat, community, or species (i.e. the components of a biotope) to return to a state close to that which existed before the activity or event caused change.
Sensitivity is dependent on the intolerance of a species or habitat to damage from an external factor and the time taken for its subsequent recovery. For example, a very sensitive species or habitat is one that is very adversely affected by an external factor arising from human activities or natural events (killed/destroyed, 'high' intolerance) and is expected to recover over a very long period of time, i.e. >10 or up to 25 years ('low'; recoverability). Intolerance and hence sensitivity must be assessed relative to change in a specific factor.

Sabellaria spinulosa

S. spinulosa is generally considered to be a very tolerant species with limited sensitivity (Table 1). Perhaps, the greatest sensitivity is to substratum loss, as once dislodged, the individual worms cannot rebuild their tubes. S. spinulosa is often one of the first species to recolonise an area after a disturbance. Therefore, this species is expected to have a high recoverability. S. spinulosa is most frequently found in polluted and disturbed conditions. S. spinulosa occurs in high densities on subtidal gravels that would be expected to be disturbed every year or perhaps once every few years due to storms and in polluted conditions. S. spinulosa appears to be very tolerant of water quality variation, but is potentially vulnerable to the short‐term and localized effects of mineral extraction and the effects of oil dispersants on the larvae.

Table 1: List of levels of “intolerance”, “recoverability” and “sensitivity” for physical and chemical threats to S. spinulosa. Level of confidence is included to give an indication of literature available on each factor. (Source: see www.marlin.ac.uk Marlin website for primary sources).
Factor Intolerance Recoverability Sensitivity Confidence
Increase in temperature Low High Low Very low
Substratum loss High High Moderate High
Increase in suspended sediment Low Immediate Not sensitive Moderate
Increase in water flow rate Intermediate High Low Moderate
Increase in turbidity Tolerant Not relevant Not sensitive Low
Increase in wave exposure Intermediate High Low Moderate
Noise Tolerant Not relevant Not sensitive Low
Abrasion & physical disturbance Intermediate High Low Low
Displacement High High Moderate Low
Decrease in salinity Intermediate High Low Moderate
Changes in oxygenation Intermediate High Low Very low


Sabellaria alveolata

Similar to S. spinulosa, recolonisation of individual S. alveolata is expected to be high, as long as there is suitable substratum for the settlement of larvae (Table 2). Recovery of reefs is expected to take considerably longer.

Table 2: List of levels of “intolerance”, “recoverability”’ and “sensitivity” for physical and chemical threats to S. alveolata. Level of confidence is included to give an indication of literature available on each factor. (Source: see www.marlin.ac.uk Marlin website for primary sources).
Factor Intolerance Recoverability Sensitivity Confidence
Increase in temperature Intermediate High Low low
Substratum loss High Moderate Moderate Low
Increase in suspended sediment Low Very high Very low Low
Increase in water flow rate Intermediate High Low Low
Increase in turbidity Tolerant Not relevant Not sensitive Low
Increase in wave exposure Intermediate High Low Low
Noise Tolerant Not relevant Not sensitive High
Abrasion & physical disturbance Intermediate High Low Moderate
Displacement High Moderate Moderate High
Decrease in salinity Intermediate High Low Low
Changes in oxygenation Intermediate High Low Very low


Mytilus spp.

It has been suggested that although mussel assemblages found in the upper intertidal or most sheltered sites experience the least change per unit time and may be considered more 'stable'[114], these assemblages would recover much slower than lower intertidal and more exposed sites if disturbed[77]. In addition, Mytilus spp. recovers quicker than other Mytilus species[77]. Overall, Mytilus spp. populations are considered to have a strong ability to recover from environmental disturbances (Table 3[74]). Larval supply and settlement could potentially occur annually, but settlement is sporadic with unpredictable pulses of recruitment[115][77]. Therefore, while good annual recruitment is possible, recovery may take at least 5 years, although in certain circumstances and under some environmental conditions, recovery may take significantly longer[116]. Establishment/recovery can fail for several reasons, including settlement limitation, post-settlement mortality, burial and physical instability[117].

Table 3: List of levels of “intolerance”, “recoverability” and “sensitivity” for physical and chemical threats to Mytilus spp.. Level of confidence is included to give an indication of literature available on each factor. (Source: see www.marlin.ac.uk Marlin website for primary sources).
Factor Intolerance Recoverability Sensitivity Confidence
Increase in temperature Low Very high Very low High
Substratum loss High High Moderate High
Increase in suspended sediment Low Immediate Not sensitive High
Decrease in emergence Low Very high Very low Low
Increase in water flow rate Low Very high Very low Moderate
Increase in turbidity Tolerant Not relevant Not sensitive Not relevant
Increase in wave exposure Intermediate High Low Moderate
Noise Tolerant* Not relevant Not sensitive Low
Abrasion & physical disturbance Intermediate High Low Moderate
Displacement Intermediate High Low Moderate
Decrease in salinity Low Very high Very low Moderate
Changes in oxygenation Low Very high Very low High


Modiolus modiolus

M. modiolus is a long‐lived species and individuals are commonly observed to be older than 25 years. This species is regarded to be intolerant of loss of substratum, physical damage and abrasion (Table 4). Recovery is thought to take many years due to sporadic recruitment[118]. M. modiolus individuals or reefs are generally not considered to be fragile, however, physical threats from fishing gears pose a significant threat to this species. Older individuals are susceptible to boring by the sponge Clione celata which can make shells brittle, thus increasing vulnerability[119].

Table 4: List of levels of “intolerance”, “recoverability” and “sensitivity” for physical and chemical threats to M. modiolus. Level of confidence is included to give an indication of literature available on each factor. (Source: See www.marlin.ac.uk Marlin website for primary sources).
Factor Intolerance Recoverability Sensitivity Confidence
Increase in temperature Intermediate Low High Very low
Substratum loss High Low High Moderate
Increase in suspended sediment Low Immediate Not sensitive Low
Increase in water flow rate Intermediate Low High Low
Increase in turbidity Low Very high Very Low Moderate
Increase in wave exposure Intermediate Low High Very low
Noise Tolerant Not relevant Not sensitive High
Abrasion & physical disturbance High Low High Low
Displacement Low Very high Very Low Very low
Decrease in salinity High Low High Moderate
Changes in oxygenation Low Very high Very low Moderate


Natural and anthropogenic threat

Physical threats can originate from natural and anthropogenic sources. Natural sources include increased temperatures, an increase in storm occurrence and intensity and sea‐level rise. In this section we holistically address the general physical pressures each species faces, rather than those from individual processes. Physical anthropogenic threats to reefs are extensive, so not all are covered in this document. Major physical threats include fishing gear, marine aggregate extraction, coastal development, construction associated with marine renewable energy, and oil and gas exploration. Natural chemical threats posed by climate change include reduced salinity, brought about by increased precipitation and surface runoff, and acidification brought about by reduced pH and changes in oxygen concentrations. Anthropogenic chemical threats are primarily those associated with pollution. Biological threats are usually considered to be natural in the form of parasites, predators and competitors. However, invasion by non‐native species is often a result of human introduction and therefore can indirectly be considered an anthropogenic threat.

Sabellaria spinulosa

Physical threats
Sabellaria spinulosa usually occurs subtidally in areas of high water flow, and is relatively tolerant of wave and tidal‐forcing. However, as S. spinulosa generally grows upon cobbles and pebbles[120], and since it has been suggested that an increase in wave or tidal flow may reduce the stability of the attachment substratum, this can result in increased scouring and mortality of individuals[121]. It is a relatively disturbance‐tolerant species and is often the first species to recolonise an area after a physical disturbance[121]. The physical disturbance of removal from tubes and substratum loss will cause mortality. As S. spinulosa is predominantly subtidal, it is likely to be less affected by temperature changes than the intertidal S. alveolata, which has been shown to be severely affected by low winter temperatures[122]. Fisheries for the pink shrimp (Pandalus montagui) and brown shrimps (Crangon crangon) (often associated with areas of Sabellaria spinulosa reefs) have been implicated in the loss or damage of reefs. However, experimental and observational studies indicated only minor damage to tubes and rapid recovery as a result of shrimp fisheries[57]. Nevertheless, populations, especially loose aggregations, may be displaced by mobile fishing gear.
Chemical threats
There is little data available on chemical threats to S. spinulosa, although it is not thought to be sensitive to reduced salinity[121].
Biological threats
There is insufficient information available on biological threats to S. spinulosa.

Sabellaria alveolata

Physical threats
Sabellaria alveolata is typically found in the intertidal and is tolerant of changes in sediment regime. The physical disturbance of removal from tubes and substratum loss will cause mortality. Being an intertidal species, the greatest threats come from cold air temperatures and heavy wave action. It has been suggested that most colonies die through eventual break up by wave action[121]. Increased exposure will result in a potentially shorter colony life. S. alveolata is a southern species and is at the northern end of its range in Britain. This species is known to be negatively affected by extremely cold winters. In the cold winter of 1962/1963, S. alveolata suffered severe mortalities along the Welsh and southern English coastlines, where it had previously reached its northern and northeastern range limits[122]. Populations suffered mortalities again during the winter of 1978/1979, but on a much smaller scale[123]. S. alveolata recolonized locations close to their northern range limits from where they were lost after the cold winter of 1962/1963[124]. Despite the current trends in global warming, winter 2009/2010 was the coldest on record in Europe, which may have negatively affected S. alveolata at its range edges. Active restoration may also be possible: transplantation experiments with S. spinulosa reef fragments showed substantial survival over 17 months, although surviving fragments did not expand significantly[125].
Chemical threats
There is insufficient information available on chemical threats to S. alveolata.
Biological threats
There is little information available on the biological threats to S. alveolata. In a study of S. alveolata reefs in the Bay of Mont San‐Michel, France, it appeared that reefs were becoming increasingly colonized by the invasive Pacific oyster Crassostrea gigas from local aquaculture operations and by green algae (Ulva spp.) due to the increasing inputs of nitrates from terrestrial origin[126]. The high filtration rates of C. gigas, may out-compete S. alveolata for food[126]. Epibionts, especially green algae, alter the population structure of S. alveolata, causing a reduction in new recruits that in the long run may degrade the reef structure itself. There is competition for space with common mussels Mytilus spp., especially on boulder scars. Heavy settlement of mussels on S. alveolata reefs are suspected of causing short term destabilization and loss of habitat[116].

Mytilus spp.

Physical threats
Mytilus spp. can be found both intertidally and subtidally. It is a fairly tolerant species with the biggest threats posed by habitat loss and dislodgement by storms[127]. Removal of the substratum, be it rock or sediment, will entail removal of the entire population and its associated community. Repeated substratum loss and recruitment result in a patchy distribution of mussels on the shore[77]. Storms and tidal surges are known to destroy mussel beds, often over hundreds of hectares in the Wash, Morecambe Bay and the Wadden Sea. With increasing wave exposure, mussel beds become increasingly patchy and dynamic. Mytilus spp. beds may also be damaged by wave driven logs or equivalent debris[77]. Trampling by human traffic is most likely in spring and summer[128]. The combined effects of trampling and natural winter disturbances may result in loss of mussel beds in the long term. Displacement and or dislodgement by storms will likely lead to mortality. Individual mussels that are swept or displaced rarely survive, as they can be buried in sand or mud, or be scattered and eaten by oystercatchers[82].
Chemical threats
In general, Mytilus spp. is tolerant of a wide range of contaminants and salinity and oxygen fluctuations. The most significant natural chemical threat to Mytilus spp. is a reduction in salinity caused by storm runoff[116]. Mussels are suspension feeders and therefore process large volumes of water together with suspended particulates and phytoplankton. Mussels absorb contaminants directly from the water, through their diet and via suspended particulate matter[129], the exact pathway is dependant on the nature of the contaminant[130].
Biological threats
Mytilus spp. host a wide variety of disease organisms, parasites and commensals from many animal and plant groups including bacteria, blue green algae, green algae, protozoa, boring sponges, boring polychaetes, boring lichen, the intermediary life stages of several trematodes, copepods and decapods[131][132]. Mytilus spp. is threatened by a number of invasive species. Aulocomya ater, a mytilid, native to South America has been reported in the Moray Firth, Scotland in 1994 and again in 1997[74][133]. A. Ater is thought to have a stronger byssal attachment than Mytilus spp. and can replace Mytilus spp. in more exposed areas if it reproduces successfully[74]. The Pacific oyster Crassostrea gigas was introduced in Europe for commercial purposes in the mid 1960s. In Europe, wild populations of Pacific oysters are already found from northern Germany to southern Portugal. Many mussel beds (Mytilus spp.) have been taken over by Pacific oysters in the Dutch Wadden Sea[134]. In the German Wadden Sea almost all mussel beds are now replaced by oyster reefs[135][136]. In the early stage of the development of C. gigas, 85% attached to Mytilus spp. (alive and empty shell) and 8% on other bivalves. The American slipper limpet Crepidula fornicata, native to the North American East coast, was unintentionally introduced to Europe by oyster farming in the 1870s and now occurs from Denmark to Spain, Norway, the Mediterranean, Ireland and the United Kingdom[137][138]. There are conflicting results in the literature on the effects of C. fornicate on Mytilus spp.. In one set of field experiments[139], the presence of C. fornicate has been shown to cause a reduction in survival and growth of the blue mussel Mytilus spp.. A reduction in survival and growth of mussels was likely due to physical interference, associated with the attachment of C. fornicata. It is probable that when attachment onto a host occurs, the host organism will experience greater drag forces, requiring them to use more energy to remain attached to the substrate. This extra energetic requirement may result in reduced fecundity and survivability. Conversely, C. fornicate have also been found to benefit Mytilus spp. The presence of C. fornicate on mussels was found to lead to a three‐fold decrease in predation by starfish[139]. Although starfish did not prey directly on C. fornicate, it is believed that the cover provided by settled limpets made it more difficult for the starfish to prey on the mussels.

Modiolus modiolus

Physical threats
M. modiolus is thought to have an intermediate to high intolerance to physical disturbance[116][118]. Subtidal M. modiolus beds are susceptible to damage from fishing activities. In Strangford Lough, Northern Ireland, M. modiolus beds have been shown to suffer damage and mortality by scallop dredging[140][141].
Chemical threats
There is insufficient information available on chemical threats to M. modiolus.
Biological threats
Predation by crabs and starfish presents one of the greatest threats to juvenile M. modiolus[142][90][118]. As mussels grow and become more difficult to open, the threat of predation becomes less important[91]. High densities of the brittle star, Ophiothrix fragilis, are considered to be capable of having a detrimental effect on M. modiolus beds not only through removal of both food and mussel larvae from the water column[45][74].

Key processes to focus on for maintaining ecosystems integrity

The distribution of biogenic reefs can change over short distances and time scales (i.e. metres and days)[143], making it difficult to accurately assess their status using point sampling methods. The ephemeral and unpredictable nature of biogenic reefs poses a challenge to effective management. The establishment of designated sites to protect habitats relies on a certain level of stability. Unless conservation effort can be concentrated on reefs of proven stability, site designation for biogenic reefs can prove unsuccessful. Some authors suggest the designation of a much broader site may be more beneficial, comprising areas which already support dense populations or are considered suitable for potential biogenic reef development[55]. This approach protects the environmental conditions and processes that allow reefs to develop. An alternative approach is the smaller-scale conservation of specific reef sites, with the view to the designation status lasting only for the lifetime of the actual reef. In order for this approach to be effective, the designation procedure must act on a shorter time scale (months rather than years) [55]. Ideally, a combination of the two above mentioned approaches would prove to be the most effective. This would involve regular mapping of biogenic reefs within a larger supporting boundary. Exclusion zones around the reefs could be established and managed.

Current management practices

The origins of legal mechanisms and targets for protecting biodiversity mostly stem from the Convention on Biological Diversity (CBD) that was drawn up in 1992. Parallel to the CBD, the European Community (EC) adopted the Council Directive 92/43/EEC in 1992, which became more commonly known as the Habitats Directive. The directive focused on the conservation of natural habitats and of wild fauna and flora through the establishment of a network of Special Areas of Conservation (SACs). Its primary objective is to protect threatened habitats and species of European importance. In response to the CBD, the UK Government also founded the UK Biodiversity Partnership to develop and implement UK Biodiversity Action Plans (UK BAP). UK BAP recognizes threatened biological assets within the UK and its surrounding waters and presents policies for the management and conservation of these assets. Plans for species and habitats in danger have been established to aid in recovery in order to assist in the UK’s development in reducing biodiversity loss set out in the CBD. This led to action plans for 1,150 priority species and 65 priority habitats. Reefs are one of the habitats listed under Annex I of the Habitats Directive which require the designation of an SAC.

Sabellaria alveolata

Intertidal protection for S. alveolata reefs can be achieved through Site of Special Scientific Interest (SSSI) designation. S. alveolata reefs also occur as sub-features of non‐reef Annex 1 habitats (eg intertidal mudflats and sandflats) under the Habitats Directive and are present in a number of Special Areas of Conservation (SACs). Discharges to the sea are controlled by a number of EC Directives, including the Dangerous Substances, Shellfish (Waters), Integrated Pollution Control, Urban Waste Water Treatment, and Bathing Waters Directives. The forthcoming Water Framework Directive will also be relevant. The Oslo and Paris Convention (OSPAR) and North Sea Conference declarations are also important. These commitments provide powers to regulate discharges to the sea and have set targets and quality standards to marine waters. An extensive set of standards covering many metals, pesticides and other toxic, persistent and bioaccumulative substances, and nutrients have been set under UK legislation.

Mytilus spp.

Although Mytilus spp. are not themselves designated for protection under these provisions, “Intertidal Mytilus spp. beds on mixed and sandy sediments” appear on the OSPAR List of Threatened and/or Declining Species and Habitats. Mytilus spp. is also protected by fisheries regulations. Fisheries regulations vary greatly in different parts of the Europe. The regulatory considerations in terms of mussel fisheries management are complex.

Modiolus modiolus

In addition to its listing by OSPAR[144], this habitat is the subject of several local, national and regional listings, including the Habitats Directive (as part of ‘Reefs’) and the UK Biodiversity Action Plan. Such listings serve to highlight the conservation needs of the habitat, but successful protection depends on specific actions that follow. In the UK M. modiolus beds are identified as features for protection in SACs (Special Areas of Conservation) off Scotland, Wales and Northern Ireland. Active restoration through hatchery production and reseeding may provide an option where natural recruitment is insufficient[113].

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Related articles

Biogenic reefs of Europe and temporal variability


References

  1. ↑ Wood, R., 1999. Reef evolution. Oxford University Press, Oxford.
  2. ↑ Roberts, J.M., Wheeler, A.J., Freiwald, A., 2006. Reefs of the deep: The biology and geology of cold-water coral ecosystems. Science 213: 543-547.
  3. ↑ Roberts, J.M., Davies, A.J., Henry, L.A., Duineveld, G., Lavaleye, M., Dodds, L.A., Maier, C., Van Soest, R.W.M., Bergman, M.I.N., Hühnerbach, V., Sinclair, D., Watmough, T., Long, D., Van Haren, H., 2009. The Mingulay reef complex, northeast Atlantic: an interdisciplinary study of cold-water coral habitat, hydrography and biodiversity. Marine Ecology Progress Series 397: 139-151.
  4. ↑ 4.0 4.1 Holt, T.J., Rees, E.I., et al. 1998. Biogenic Reefs (volume IX). An overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scottish Association for Marine Science (UK Marine SACs Project). 170 Pages.
  5. ↑ Foster-Smith, R.L., Hendrick, V.J., 2003. Sabellaria spinulosa reef in The Wash and North Norfolk cSAC and its approaches: Part III, Summary of knowledge, recommended monitoring strategies and outstanding research requirements. English Nature Research Reports, 543.
  6. ↑ Hendrick, V.J., Foster-Smith, R.L., 2006. Sabellaria spinulosa reef: a scoring system for evaluating 'reefiness' in the context of the Habitats Directive. Journal of the Marine Biological Association of the United Kingdom 86: 665-677.
  7. ↑ 7.0 7.1 7.2 Wilson, D. P., 1971. Sabellaria colonies At Duckpool, North Cornwall, 1961-1970. Journal of the Marine Biological Association of the UK 51: 509-580.
  8. ↑ 8.0 8.1 8.2 8.3 Gruet, Y., 1982. Recherches sur lécologie des récifs d'Hermelles édicés par lAnnélide Polychète Sabellaria alveolata (Linné), Université des Sciences et Techniques, Nantes, France. PhD.
  9. ↑ 9.0 9.1 Cunningham, P.N., Hawkins, S.J., Jones, H.D., Burrows, M.T., 1984. The geographical distribution of Sabellaria alveolata (L.) in England, Wales and Scotland, with investigations into the community structure of, and the effects of trampling on Sabellaria alveolata colonies. Report to the Nature Conservancy Council from the Department of Zoology, Manchester University, Manchester.
  10. ↑ Mettam, C., Conneely, M.E., White, S.J., 1994. Benthic macrofauna and sediments in the Severn Estuary. Biological Journal of the Linnaean Society 51: 71-81.
  11. ↑ Perkins, E.J., Abbott, O.J., Nottage, A.S., Reid, D.M., Lampard, D.J., 1980. Sixth annual report to the Cumbria Sea-Fisheries Committee. Solway Firth survey - 1st April 1979 to 31st March 1980. University of Strathclyde, Department of Biology.
  12. ↑ Marchand, Y., Cazoulat, R., 2003. Biological reef survey using spot satellite data classification by cellular automata method - Bay of Mont Saint-Michel (France). Computers & Geosciences 29: 413-421.
  13. ↑ Poloczanska, E.S., Hughes, D.J., Burrows, M.T., 2004. Underwater television observations of Serpula vermicularis (L.) reefs and associated mobile fauna in Loch Creran, Scotland. Estuarine. Coastal and Shelf Science 61: 425-435.
  14. ↑ Dodd, J., Baxter, L., Hughes, D., 2009. Mapping Serpula vermicularis (Polychaeta: Serpulidae) aggregations in Loch Teacuis, western Scotland, a new record. Mar Biol Res 5: 200-205.
  15. ↑ Schroder, L., Lam-Gordillo, O. and Dittmann, S. 2024. Classification, density, and spatial distribution of polychaete reefs in the Coorong, South Australia. Estuarine, Coastal and Shelf Science 306: 108905
  16. ↑ McQuaid, K.A. and Griffiths, C.L. 2014. Alien reef-building polychaete drives long-term changes in invertebrate biomass and diversity in a small, urban estuary. Estuarine Coastal Shelf Sci 138: 101–106
  17. ↑ Brundu, G. and Magni, P. 2021. Context-dependent effect of serpulid reefs on the variability of soft-bottom macrobenthic assemblages in three Mediterranean lagoons (Sardinia, Italy). Estuarine Coastal and Shelf Sci 262: 107589
  18. ↑ Charles, M., Faillettaz, R., Desroy, N., Fournier, J. and Costil, K. 2018. Distribution, associated species and extent of biofouling reefs formed by the alien species Ficopomatus enigmaticus (Annelida, Polychaeta) in marinas. Estuarine Coastal and Shelf Sci 212: 164–175
  19. ↑ 19.0 19.1 Dankers, N., Brinkman, A.G., Meijboom, A., Dijkman, E., 2001. Recovery of intertidal mussel beds in the Waddensea: use of habitat maps in the management of the fishery. Hydrobiologia 465: 21–30.
  20. ↑ Commito, J.A., Rusignuolo, B.R., 2000. Structural complexity in mussel beds: the fractal geometry of surface topography. Journal of Experimental Marine Biology and Ecology 255: 133–152.
  21. ↑ Commito, J.A., Dankers, N., 2001. Dynamics of spatial and temporal complexity in European and North American softbottom mussel beds. In: Reise, K. (Editor). Ecological Comparisons of Sedimentary Shores. Springer-Verlag, Heidelberg, 39–59.
  22. ↑ 22.0 22.1 22.2 Widdows, J., Brinsley, M.D., 2002. Impact of biotic and abiotic processes on sediment dynamics and the consequences to the structure and functioning of the intertidal zone. Journal of Sea Research 48: 143–156.
  23. ↑ 23.0 23.1 Widdows, J., Donkin, P., Staff, F.J., Matthiessen, P., Law, R.J., Allen, Y.T., Thain, J.E., Allchin, C.R., Jones, B.R., 2002. Measurement of stress effects (scope for growth) and contaminant levels in mussels (Mytilus spp.) collected from the Irish Sea. Marine Environmental Research 53: 327–356.
  24. ↑ Gutiérrez, J.L., Jones, C.G., Strayer, D.L., Iribarne, O.O., 2003. Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101: 79–90.
  25. ↑ 25.0 25.1 Flemming, B.W., Delafontaine, M.T., 1994. Biodeposition in a juvenile mussel bed of the East Frisian Wadden Sea (southern North Sea). Netherlands Journal of Aquatic Ecology 28: 289–297.
  26. ↑ Oost, A.P., 1995. The influence of biodeposits of the blue mussel Mytilus spp. on fine-grained sedimentation in the temperate-climate Dutch Wadden Sea. Geologica Ultraiectina 126: 359-400.
  27. ↑ Sampaio, L., Moreira, J., Rubal, M., Guerrero-Meseguer, L. and Veiga, P. 2022. A review of coastal anthropogenic impacts on mytilid mussel beds: Effects on mussels and their associated assemblages. Diversity 14: 409
  28. ↑ Jackson J., 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. The American Naturalist 111: 743-767.
  29. ↑ Wood R., 1999. Reef Evolution. Oxford University Press, Oxford. pp. 414.
  30. ↑ Chisholm J.R.M. and Kelley R., 2001. Worms start the reef-building process. Nature 409: 152 153.
  31. ↑ 31.0 31.1 Connor D., Dalkin M., Hill T., Holt R. and Sanderson W., 1997. Marine Nature Conservation Review: marine biotope classification for Britain and Ireland. Volume 2. Sublittoral biotopes. Version 97.06. Joint Nature Conservation Committee, Peterborough. pp 448.
  32. ↑ Holt T., Hartnoll R. and Hawkins S., 1997. Sensitivity and vulnerability to man‐induced change of selected communities: intertidal brown algal shrubs, Zostera beds and Sabellaria spinulosa reefs. English Nature Research Reports. No. 234. pp97.
  33. ↑ Warren P.J., Sheldon R.W., 1967. Feeding and migration patterns of the Pink Shrimp Pandalus montagui, in the estuary of the River Crouch, England, Journal of the Fisheries Research Board of Canada 24: 569-580.
  34. ↑ 34.0 34.1 Schafer W., 1972. Ecology and Palaeoecology of Marine Environments. Translation of Aktuo-paläontologie nach Studien in der Nordsee. University of Chicago Press, Chicago. pp 568.
  35. ↑ Warren P., 1973. The fishery for the pink shrimp Pandalus montagui of the Wash. Laboratory Leaflet (New Series) No. 28. Ministry of Agriculture, Fisheries and Food, Lowestoft. pp. 46.
  36. ↑ Limpenny D.S., Foster‐Smith R.L., Edwards T.M., Hendrick V.J., Diesing M., Eggleton J.D., Meadows W.J., Crutchfield Z., Pfeifer S. and Reach I.S., 2010. Best methods for identifying and evaluating Sabellaria spinulosa and cobble reef. Aggregate Levy Sustainability Fund Project MAL0008. Joint Nature Conservation Committee, Peterborough. pp 134.
  37. ↑ van der Reijden, K.J., Koop, L., Mestdagh, S., Snellen, M., Herman, P.M.J., Olff, H. and Govers, L.L. 2021. Conservation implications of Sabellaria spinulosa reef patches in a dynamic sandy-bottom environment. Front. Mar. Sci 8: 642659
  38. ↑ Kirtley D.J., 1992. Built to last. Worm reefs. A feat of natural engineering. Florida Oceanographic Magazine 13: 12‐19.
  39. ↑ Jones L., 1999. Habitat Action Plan: Sabellaria spinulosa reefs. English Nature. pp 4.
  40. ↑ Jones L.A., Hiscock K., Connor D.W., 2000. Marine habitat reviews. A summary of ecological requirements and sensitivity characteristics for the conservation and management of marine SACs. Joint Nature Conservation Committee, Peterborough. (UK Marine SACs Project report).
  41. ↑ Foster‐Smith R.L., 2001. Report of the field survey for the 2001 Sabellaria spinulosa project. A report for the Eastern Sea Fisheries Joint Committee and English Nature. pp 45.
  42. ↑ Cooper, K.M. et al. 2022. Seabed morphology and bed shear stress predict temperate reef habitats in a high energy marine region. Estuar. Coast. Shelf Sci 274: 107934
  43. ↑ Baptist, M.J. 2026. Historic occurrence and habitat preference of the reef-building polychaete Sabellaria spinulosa in the Wadden Sea. Journal of Sea Research 211: 102693
  44. ↑ Caspers H., 1950. Die Lebensgemeinschaft der Helgolander Austernbank. Helgoland Marine Research 3: 119-169].
  45. ↑ 45.0 45.1 45.2 45.3 George C. and Warwick R., 1985. Annual production in a hard‐bottom reef community. Journal of the Marine Biological Association of the United Kingdom 65: 713-735.
  46. ↑ 46.0 46.1 Jessop R. and Stoutt J., 2006. Broad scale Sabellaria spinulosa distribution in the central Wash (Southern North Sea), as predicted with the acoustic ground discriminating system (A.G.D.S) RoxannTM. Draft report by the Eastern Sea Fisheries Joint Committee for English Nature. pp 26.
  47. ↑ 47.0 47.1 Linke O., 1951. Neue Beobachtungen uber Sandkorallen‐Riffe in der Nordsee, Natur u.Volk 81: 77-84.
  48. ↑ 48.0 48.1 48.2 Wilson D.P., 1971. Sabellaria colonies At Duckpool, North Cornwall, 1961‐1970. Journal of the Marine Biological Association of the UK, 51: 509‐580.
  49. ↑ Michaelis H., 1978. Recent biological phenomena in the German Waddensea. Symposium on North Sea fish stocks-recent changes and their causes., Aarhus (Denmark).
  50. ↑ 50.0 50.1 50.2 Eckelbarger K.J., 1978. Metamorphosis and settlement in the Sabellariidae. In: Chai, F.-S. & Rice, M. (Eds.). Settlement and Metamorphosis of Marine Invertebrate Larvae.Proceedings of the Symposium on Settlement and Metamorphosis of Marine Invertebrate Larvae, American Zoological Society Meeting. Totonto, Ontario, Canada December 27-28, 1977. Elsevier, New York: 145-164.
  51. ↑ Wilson D.P., 1929. The larvae of the British Sabellarians. Journal of the Marine Biological Association of the United Kingdom 15: 221‐269.
  52. ↑ 52.0 52.1 52.2 52.3 Wilson D.P., 1968.The settlement behavior of the larvae of Sabellaria alveolata. Journal of the Marine Biological Association of the United Kingdom 48: 387‐435.
  53. ↑ Wilson D.P., 1970. The larvae of Sabellaria Spinulosa and their settlement behaviour. Journal of the Marine Biological Association of the United Kingdom 50: 33-52.
  54. ↑ Jensen R.A., 1992. Marine bioadhesive: role for chemosensory recognition in a marine invertebrate. Biofouling 5: 177-193.
  55. ↑ 55.0 55.1 55.2 Hendrick V. J., Foster‐Smith R. L. and Davies A. J., 2011. Biogenic Reefs and the Marine Aggregate Industry. Marine ALSF Science Monograph Series No. 3. MEPF 10/P149. (Edited by R. C. NEWELL & J. MEASURES). 60pp. ISBN: 978 0 907545 46 0. Cite error: Invalid <ref> tag; name "Hendrick" defined multiple times with different content
  56. ↑ Davies A.J., Last K.S., Attard K., Hendrick V.J., 2009. Maintaining turbidity and current flow in laboratory aquarium studies, a case study using Sabellaria spinulosa. Journal of Experimental Marine Biology and Ecology 370: 35-40.
  57. ↑ 57.0 57.1 Vorberg R., 2000. Effects of the shrimp fisheries on reefs of Sabellaria spinulosa (Polychaeta). ICES Journal of Marine Science 57: 1416-1420.
  58. ↑ Stewart R.J., Weaver J.C., Morse D.E. and Waite J.H., 2004. The tube cement of Phragmatopoma californica: a solid foam. Journal of Experimental Biology 207: 4727-4734.
  59. ↑ Braithwaite C.J.R., Robinson R.J. and Jones G., 2006. Sabellarids: a hidden danger or an aid to subsea pipelines? Quarterly Journal of Engineering Geology and Hydrogeology 39: 259‐265.
  60. ↑ Last K.S., Hendrick V.J., Beveridge C.M. and Davies A.J., 2011. Measuring the effects of suspended particulate matter and smothering on the behaviour, growth and survival of key species found in areas associated with aggregate dredging. Report for the Marine Aggregate Levy Sustainability Fund, Project MEPF 08/P76. 69 pp.
  61. ↑ Kirtley D.J., 1966. Intertidal reefs of Sabellariidae (Annelida polychaeta) along the coasts of Florida. Masters thesis. The Florida State University. Tallahassee, Florida. 104 pp. Original reference not seen. Cited by Drake, C.A., McCarthy, D.A. & von Dohlen, C.D. (2007). Molecular relationships and species divergence among Phragmatopoma spp. (Polychaeta: Sabellaridae) in the Americas. Marine Biology 150: 345‐358.
  62. ↑ Mccarthy D., 2001. Life-history patterns and the role of disturbance in intertidal and subtidal populations of the polychaete Phragmatopoma lapidosa lapidosa (Kinberg, 1867) in the tropical Western Atlantic. PhD Thesis. Kings College, University of London. Original reference not seen. Cited by Drake, C.A., McCarthy, D.A. & von Dohlen, C.D. (2007).Molecular relationships and species divergence among Phragmatopoma spp. (Polychaeta: Sabellaridae) in the Americas. Marine Biology 150: 345‐ 358.
  63. ↑ Mccarthy D., Young C. and Emson R., 2003. Influence of wave-induced disturbance on seasonal spawning patterns in the sabellariid polychaete Phragmatopoma lapidosa. Marine Ecological Progress Series 256: 123-133.
  64. ↑ Wilson D.P., 1974. Sabellaria Colonies at Duckpool, North Cornwall, 1971–1972, With a Note for May 1973. Journal of the Marine Biological Association of the United Kingdom 54: 393‐436.
  65. ↑ 65.0 65.1 65.2 65.3 Cunningham P.N., Hawkins S.J., Jones H.D., Burrows M.T., 1984. The geographical distribution of Sabellaria alveolata (L.). In: England, Wales and Scotland, with investigations into the community structure of, and the effects of trampling on Sabellaria alveolata colonies. Report to the Nature Conservancy Council from the Department of Zoology, Manchester University, Manchester. NCC report No. HF3/11/22.
  66. ↑ Larsonneur C. 1994. The Bay of Mont‐Saint‐Michel: A sedimentation model in a temperate macrotidal environment. Senckenbergiana maritima 24: 3‐63.
  67. ↑ Mieszkowska, N. et al. 2023. Northward range expansions are not the full story: A case study of Sabellaria alveolata in Great Britain. Estuar. Coast. Shelf Sci 294: 108543
  68. ↑ Wilson D.P., 1976. Sabellaria Alveolata (L.) At Duckpool, North Cornwall, 1975. Journal of the Marine Biological Association of the United Kingdom 56: 305-310.
  69. ↑ 69.0 69.1 Gruet Y., 1982. Recherches sur l’écologie des récifs d’Hermelles édicés par l’Annélide Polychète Sabellaria alveolata (Linné), Université des Sciences et Techniques, Nantes, France. PhD.
  70. ↑ Schroder, L., Lam-Gordillo, O. and Dittmann, S. 2024. Classification, density, and spatial distribution of polychaete reefs in the Coorong, South Australia. Estuarine, Coastal and Shelf Science 306: 108905
  71. ↑ McQuaid, K.A. and Griffiths, C.L. 2014. Alien reef-building polychaete drives long-term changes in invertebrate biomass and diversity in a small, urban estuary. Estuarine Coastal Shelf Sci 138: 101–106
  72. ↑ Brundu, G. and Magni, P. 2021. Context-dependent effect of serpulid reefs on the variability of soft-bottom macrobenthic assemblages in three Mediterranean lagoons (Sardinia, Italy). Estuarine Coastal and Shelf Sci 262: 107589
  73. ↑ Charles, M., Faillettaz, R., Desroy, N., Fournier, J. and Costil, K. 2018. Distribution, associated species and extent of biofouling reefs formed by the alien species Ficopomatus enigmaticus (Annelida, Polychaeta) in marinas. Estuarine Coastal and Shelf Sci 212: 164–175
  74. ↑ 74.00 74.01 74.02 74.03 74.04 74.05 74.06 74.07 74.08 74.09 74.10 Holt T.J., Rees E.I., Hawkins, S.J., Seed, R., 1998. Biogenic Reefs (volume IX). An overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scottish Association for Marine Science (UK Marine SACs Project). 170 pp.
  75. ↑ 75.0 75.1 Seed R., 1969. The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores. Oecologia 3: 317‐350.
  76. ↑ Roberts D. and Mckenzie J.D., 1983. Utilisation of mollusk resources in N. Ireland. Journal of Molluscan Studies 49: 162-166.
  77. ↑ 77.0 77.1 77.2 77.3 77.4 77.5 Seed R. and Suchanek T.H., 1992. Population and community ecology of Mytilus. In: Gosling, E. (Ed.). The mussel Mytilus: ecology, physiology, genetics and culture. Developments in Aquaculture and Fisheries Science. 25, Elsevier, Amsterdam: 87-170.
  78. ↑ Widdows J. and Shick J.M., 1985. Physiological responses of Mytilus edulis and Cardium edule to aerial exposure. Marine Biology 85: 217-232.
  79. ↑ 79.0 79.1 Mcgrath D., King P. and Gosling E., 1988. Evidence for the direct settlement of Mytilus edulis larvae on adult mussel beds. Marine Ecological Progress Series 47: 103‐106.
  80. ↑ Pulfrich, A., 1996; Attachment and settlement of post-larval mussels (Mytilus edulis L) in the Schleswig-Holstein Wadden Sea Source. Journal of Sea Research 36: 239-250
  81. ↑ Beukema, J.J. (1981). Quantitative data on the benthos of the Wadden Sea proper. In: Dankers, N.M.J.A. et al. (1981).Invertebrates of the Wadden Sea: final report of the section 'Marine Zoology' of the Wadden Sea Working Group. Wadden Sea Working Group Report, 4: 134-142.
  82. ↑ 82.0 82.1 Dare P.J., 1976. Settlement, growth and production of the mussel, Mytilus edulis L., in Morecambe Bay, England. Fishery Investigations, Ministry of Agriculture, Fisheries and Food. Pp 25.
  83. ↑ Seed R., 1976. Ecology. In: Bayne, B. (Ed.). Marine mussels: their ecology and physiology. International Biological Programme 10. Cambridge University Press, Cambridge: pp. 13‐66.
  84. ↑ Sukhotin A.A., Strelkov P.P., Maximovich N.V. and Hummel H., 2007. Growth and longevity of Mytilus edulis (L.) from northeast Europe. Marine Biology Research 3: 155-167.
  85. ↑ Holt T.J. and Shalla S.H.A., 1997. Pre- and post-drilling survey of block IOM 112/19, A report to Elf Enterprise Caledonia Ltd. By Port Erin Marine Laboratory, University of Liverpool. Unpublished work.
  86. ↑ Schweinitz E. and Lutz R., 1976. Larval development of the northern horse mussel, Modiolus modiolus (L.), including a comparison with the larvae of Mytilus edulis L. as an aid in planktonic identification. Biological Bulletin 150: 348‐360.
  87. ↑ 87.0 87.1 Davenport J. and Kjorsvik E., 1982. Observations on a Norwegian intertidal population of the horse mussel Modiolus modiolus (L.). Journal of Molluscan Studies 48: 370‐371.
  88. ↑ Coleman N.,1976. Aerial respiration of Modiolus modiolus. Comparative Biochemistry and Physiology Part A: Physiology 54: 401‐406.
  89. ↑ Wildish D.J., Fader G. and Parrott D., 2009. A model of horse mussel reef formation in the Bay of Fundy based on population growth and geological processes. Atlantic Geology 45: 157-170.
  90. ↑ 90.0 90.1 Anwar N. A., Richardson C.A. and Seed R., 1990. Age determination, growth rate and population structure of the horse mussel Modiolus modiolus. Journal of the Marine Biological Association of the United Kingdom 70: 441-457.
  91. ↑ 91.0 91.1 Seed R. and Brown R.A., 1977. Comparison of reproductive cycles of Modiolus modiolu (L), Cerastoderma (= Cardium) edule (L), and Mytilus edulis L in Strangford Lough, Northern Ireland. Oecologia 30: 173-188.
  92. ↑ 92.0 92.1 Brown R.A. 1984. Geographical variations in the reproduction of the horse mussel, Modiolus modiolus (Mollusca: bivalvia). Journal of the Marine Biological Association of the United Kingdom 64: 751-770.
  93. ↑ Jasim A.K. and Brand A.R., 1989. Observations on the reproduction of Modiolus modiolus in Isle of Man waters. Journal of the Marine Biological Association of the UK 69: 373-385.
  94. ↑ Bianchi, C.N., 2001. La biocostruzione negli ecosistemi marini e la biologia marina Italiana. Biologia Marina Mediterranea 8: 112-130.
  95. ↑ Dubois, S., et al., 2002. Biodiversity associated with Sabellaria alveolata (Polychaeta: Sabellariidae) reefs: effects of human disturbances. Journal of the Marine Biological Association of the UK 82: 817-826.
  96. ↑ O'Connor, N.E., Crowe, T.P., 2007. Biodiversity among mussels: separating the influence of sizes of mussels from the ages of patches. Journal of the Marine Biological Association of the United Kingdom 89: 551-557.
  97. ↑ 97.0 97.1 97.2 Jackson, A., Hiscock, K., 2008. Sabellaria spinulosa. Ross worm. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on-line]. Plymouth: Marine Biological Association of the United Kingdom. [cited 28/04/2010]. Available from: [1]
  98. ↑ Hendrick, V.J., Foster-Smith, R.L., 2006 Sabellaria spinulosa reef: a scoring system for evaluating 'reefiness' in the context of the Habitats Directive. Journal of the Marine Biological Association of the United Kingdom 86: 665-677.
  99. ↑ Davies, A.J., Last, K.S., Attard, K., Hendrick, V.J., 2009. Maintaining turbidity and current flow in laboratory aquarium studies, a case study using Sabellaria spinulosa. Journal of Experimental Marine Biology and Ecology 370: 35-40.
  100. ↑ Fager, E.W., 1964. Marine Sediments: Effects of a Tube-Building Polychaete. Science 143: 356-358.
  101. ↑ Gram, R., 1968. A Florida Sabellaridae reef and its effect on sediment distribution. J. Sediment. Petrol., 38: 863- 868.
  102. ↑ Multer, H.G., Milliman, J.G., 1967. Geologic aspects of sabellarian reefs, Southeastern Florida. Bulletin of Marine Science. 17. p257- 267.
  103. ↑ Naylor, L.A., Viles, H.A., 2000. A temperate reef builder: an evaluation of the growth, morphology and composition of Sabellaria alveolata (L.) colonies on carbonate platforms in South Wales. In: E.R. Insalaco, P.W. Skelton and T.J. Palmer (Eds), 2000. Carbonate platform systems: components and interactions. Spec. Publ.-Geol. Soc. Lond. vol 178: 9–19.
  104. ↑ Naylor, L.A., 2001. An assessment of the links between biogenic processes and shore platform geomorphology. Glamorgan Heritage Coast, South Wales, UK. Thesis, D. Phil., University of Oxford.
  105. ↑ Jones, A.G., Denis, L., Fournier, J., Desroy, N., Duong, G. and Dubois, S.F. 2020. Linking multiple facets of biodiversity and ecosystem functions in a coastal reef habitat. Marine Environmental Research 163: 105092
  106. ↑ Crisp, D.J., 1964. The effects of the severe winter of 1962-63 on marine life in Britain. Journal of Animal Ecology. 33: 165-210.
  107. ↑ Beukema, J.J., Cadée, G.C., 1996. Consequences of the sudden removal of nearly all mussels and cockles from the Dutch Wadden Sea. PSZN Mar Ecol 17: 279–289.
  108. ↑ van Katwijk, M.M., 2003. Reintroduction of eelgrass (Zostera marina L.) in the Dutch Wadden Sea, a research overview and management vision. 173-197. In: Challenges to the Wadden Sea area. Wolff W.J., K. Essink, A. Kellermann and M.A. van Leeuwe (Eds). Proceedings of the 10th International Scientific Wadden Sea Symposium.
  109. ↑ De Vries, M.B., Bouma, T.J., van Katwijk, M.M., Borsje, B.W., Van Wesenbeeck, B.K., 2007. Biobouwers van de kust. Report Z4158. WL|Delft Hydraulics, Delft, The Netherlands.
  110. ↑ van Leeuwen, B., Augustijn, D.C.M., et al., 2010. Modeling the influence of a young mussel bed on fine sediment dynamics on an intertidal flat in the Wadden Sea. Ecological Engineering 36: 145-153.
  111. ↑ Seed, R., Suchanek T.H., 1992. Population and community ecology of Mytilus. Amsterdam, Elsevier Science Publ.
  112. ↑ Odum, H.T., Odum, B., 2003. Concepts and methods of ecological engineering. Ecological Engineering 20: 339–361.
  113. ↑ 113.0 113.1 Fariñas-Franco, J.M., Cook, R.L., Gell, F.R., Harries, D.B., Hirst, N., Kent, F., MacPherson, R., Moore, C., Mair, J.M., Porter, J.S. and Sanderson, W.G. 2023. Are we there yet? Management baselines and biodiversity indicators for the protection and restoration of subtidal bivalve shellfish habitats. Science of the Total Environment 863: 161001
  114. ↑ Lewis, 1977: The role of physical and biological factors in the distribution and stability of rocky shore communities Lewis, J.R. (1977). The role of physical and biological factors in the distribution and stability of rocky shore communities. In: Keegan, B.F. et al. (Ed.) (1977). Biology of Benthic Organisms: 11th European Symposium on Marine Biology, Galway, 1976. 417-424.
  115. ↑ Lutz R.A. and Kennish M.J., 1992. Ecology and morphology of larval and early postlarval mussels. In: Gosling, E. (Ed.). The mussel Mytilus: ecology, physiology, genetics and culture. Developments in Aquaculture and Fisheries Science 25. Elsevier Press, Amsterdam: pp. 53‐86.
  116. ↑ 116.0 116.1 116.2 116.3 Tyler-walters H., 2008. Mytilus edulis. Common mussel. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on‐line]. Plymouth: Marine Biological Association of the United Kingdom.
  117. ↑ Temmink, R.J.M., Fivash, G.S., Govers, L.L., Nauta, J., Marin-Diaz, B., Cruijsen, P.M.J.M., Didderen, K., Penning, E., Olff, H., Heusinkveld, J.H.T., Lamers, L.P.M., Lengkeek, W., Christianen, M.J.A., Reijers, V.C., Bouma, T.J. and van der Heide, T. 2022. Initiating and upscaling mussel reef establishment with life cycle informed restoration: Successes and future challenges. Ecological Engineering 175: 106496
  118. ↑ 118.0 118.1 118.2 Tyler-walters H., 2007. Modiolus modiolus. Horse mussel. Marine Life Information Network: Biology and Sensitivity Key Information Sub‐programme [on-line]. Plymouth: Marine Biological Association of the United Kingdom. [cited 01/05/2011]. more info: www.marlin.ac.uk.
  119. ↑ Comely C.A. 1978. Modiolus modiolus (L.) from the Scottish west coast. Ophelia 17: 167-193.
  120. ↑ Connor D.W., Allen J.H., Golding N., Howell K.L. Lieberknecht L.M., Northen K.O. and Reker J.B., 2004. The Marine Habitat Classification for Britain and Ireland. Version 04.05 (internet version: www.jncc.gov.uk). Joint Nature Conservation Committee, Peterborough
  121. ↑ 121.0 121.1 121.2 121.3 Jackson A. and Hiscock K., 2008. Sabellaria spinulosa. Ross worm. Marine Life Information Network: Biology and Sensitivity Key Information Sub‐programme [on-line]. Plymouth: Marine Biological Association of the United Kingdom. Available from: www.marlin.ac.uk.
  122. ↑ 122.0 122.1 Crisp D.J. 1964. The effects of the severe winter of 1962‐63 on marine life in Britain. Journal of Animal Ecology 33: 165‐210.
  123. ↑ Kendall M.A. and Bedford M.L., 1987. Reproduction and recruitment in the barnacle Chthamalus montaguiat Aberystwyth (mid-Wales). Marine Ecology Progress Series 38: 305-308.
  124. ↑ Mieszkowska N., Kendall M.A., Hawkins S.J., Leaper R., Williamson P., Hardman-Mountford N.J., Southward A.J., 2006. Changes in the range of some common rocky shore species in Britain - a response to climate change? Hydrobiologia 555: 241‐51.
  125. ↑ Franzitta, G., Colletti, A., Savinelli, B., Lo Martire, M., Corinaldesi, C. and Musco, L. 2022. Feasibility of the Sabellarid Reef Habitat Restoration. Front. Mar. Sci 9: 854986
  126. ↑ 126.0 126.1 Dubois S., Commito J.A., Olivier F. and Retiere C., 2006. Effects of epibionts on Sabellaria alveolata (L.) biogenic reefs and their associated fauna in the Bay of Mont Saint-Michel. Estuarine, Coastal and Shelf Science 68: 635‐646.
  127. ↑ Banke, T.L., Steinfurth, R.C., Lange, T., Canal-Vergés, P., Svane, N. and Flindt, M.R. 2024. Dislodgement and mortality challenges when restoring shallow mussel beds (Mytilus edulis) in a Danish estuary. Restoration Ecology 32: e14160
  128. ↑ Brosnan D.M. and Crumrine L.L., 1994. Effects of human trampling on marine rocky shore communities. Journal of Experimental Marine Biology and Ecology 177: 79-97.
  129. ↑ Widdows J. and Donkin P., 1992. Mussels and environmental contaminants: bioaccumulation and physiological aspects. In: Gosling, E. (Ed.). The mussel Mytilus: ecology, physiology, genetics and culture. Developments in Aquaculture and Fisheries Science 25. Elsevier Press, Amsterdam: pp.383‐424.
  130. ↑ Livingstone D.R. and Pipe R.K., 1992. Mussels and environmental contaminants: molecular and cellular aspects. In: Gosling, E. (Ed.). The mussel Mytilus: ecology, physiology, genetics and culture. Developments in Aquaculture and Fisheries Science 25. Elsevier Press, Amsterdam: 425-510.
  131. ↑ Bower S.M., 1992. Diseases and parasites of mussels. In: Gosling, E. (Ed.). The mussel Mytilus: ecology, physiology, genetics and culture. Developments in Aquaculture and Fisheries Science 25. Elsevier, Amsterdam: pp. 543‐563.
  132. ↑ Gray A.P., Lucas I.A.N., Seed R. and Richardson C.A., 1999 Mytilus edulis chilensis infested with Coccomyxa parasitica (Chlorococcales, Coccomyxaceae). Journal of Molluscan Studies 65: 289-294.
  133. ↑ Mckay D., 1994. Unravelling the choreography of contaminant kinetics: approaches to quantifying the uptake of chemicals by organisms. In: J.L. Hamelink, P.F. Landrum, H.L. Bergman and W.H. Benson (Editors), Bioavailability: Physical, Chemical, and Biological Interactions, Lewis Publisher Inc., Chelsea, MI., pp. 17l‐l77.
  134. ↑ Fey F., Danker N., Steenbergen J. and Goudswaard K., 2010. Development and distribution of the non-indigenous Pacific oyster (Crassostrea gigas) in the Dutch Wadden Sea. Aquaculture International 18: 45‐59.
  135. ↑ Nehls G., Diederich S., Thieltges D. and Strasser M., 2006. Wadden Sea mussel beds invaded by oysters and slipper limpets: competition or climate control? Helgoland Marine Research 60: 135‐143.
  136. ↑ Wehrmann A, Markert A, Schmidt A., 2007 Miesmuschelbank: ein verlorener Lebensraum? Die Einwanderung der Pazifischen Auster in das Wattenmeer und ihre Folgen. Natur- und Umweltschutz 6: 10–14.
  137. ↑ Blanchard M., 1997. Spread of the slipper‐limpet (Crepidula fornicata) in Europe. Current state and consequences. Scientia Marina.61(2 sup.): 109-118.
  138. ↑ Thieltges D.W., Strasser M., Reise K., 2003. The American slipper limpet Crepidula fornicate (L.) in the northern Wadden Sea 70 years after its introduction. Helgoland Marine Research 57: 27-33.
  139. ↑ 139.0 139.1 Thieltges D.W., 2005a. Impact of an invader: epizootic American slipper limpet Crepidula fornicate reduces survival and growth in European mussels. Marine Ecology Progress Series 286: 13-19.
    Thieltges, D.W., 2005b. Benefit from an invader: American slipper limpet Crepidula fornicate reduces star fish predation on basibiont European mussels. Hydrobiologia 541: 241‐244.
  140. ↑ Service M., Magorrian B. H., 1997. The extent and temporal variation of disturbance of epibenthic communities in Strangford Lough, Northern Ireland. Journal of the Marine Biological Association of the United Kingdom 77: 1151‐1164.
  141. ↑ Magorrian B.H. and Service, M., 1998. Analysis of underwater visual data to identify the impact of physical disturbance on horse mussel (Modiolus modiolus) beds. Marine Pollution Bulletin 36: 354-359.
  142. ↑ Brown R.A. and Seed R., 1977. Modiolus modiolus (L.) - an autecological study. In: Keegan, B.F., O'Ceidigh, P., Boaden, P.J.S. (eds). Biology of Benthic Organisms. Proceedings of the 11th European Symposium on Marine Biology, Pergamon Press, Oxford, Galway, Ireland, pp 93‐100.
  143. ↑ Foster‐Smith R.L., 2000. Establishing a monitoring baseline for the Wash subtidal sandbanks. pp 51.
  144. ↑ OSPAR Commission 2025. Status Assessment 2025 – Modiolus modiolus beds. OSPAR Commission, Publication 1080
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