The Marine Life Information Network

Temperature increase (local)

Benchmark. A 5°C increase in temperature for one month, or 2°C for one year. Further detail

Evidence

The barnacle Semibalanus balanoides is primarily a ‘northern’ species with an arctic-boreal distribution. Long-term time series show that recruitment success is correlated to sea temperatures (Mieszkowska, et al., 2014) Due to warming temperatures its range has been contracting northwards. Temperatures above 10 to 12 ^oC inhibit reproduction (Barnes, 1957, 1963, Crisp & Patel, 1969) and laboratory studies suggest that temperatures at or below 10^oC for 4-6 weeks are required in winter for reproduction, although the precise threshold temperatures for reproduction are not clear (Rognstad et al., 2014). Observations of recruitment success in Semibalanus balanoides throughout the South West of England, strongly support the hypothesis that an extended period (4-6 weeks) of sea temperatures <10 ^oC is required to ensure a good supply of larvae (Rognstad et al., 2014, Jenkins et al., 2000). Adults may be able to tolerate an acute or chronic change, however, if an acute change in temperature occurred in winter it could disrupt reproduction while a chronic change could alter reproductive success if it exceeded thermal thresholds for reproduction. The effects would depend on  the magnitude, duration, and footprint of the activities leading to this pressure. During periods of high reproductive success linked to cooler temperatures the range of barnacles can increase with range extensions in the order of 25 km (Wethey et al., 2011), and 100 km (Rognstad et al., 2014) were observed.

Mytilus edulis is a eurytopic species found in a wide temperature range from mild, subtropical regions to areas which frequently experience freezing conditions and are vulnerable to ice scour (Seed & Suchanek 1992).  In British waters 29°C was recorded as the upper sustained thermal tolerance limit for Mytilus edulis (Read & Cumming, 1967; Almada-Villela, et al., 1982), although it is thought that European mussels will rarely experience temperatures above 25°C (Seed & Suchanek, 1992). At the upper range of a mussels tolerance limit, heat shock proteins are produced, indicating high stress levels (Jones et al., 2010).  After a single day at 30°C, heat shock proteins were still present over 14 days later, although at a reduced level.  Increased temperatures can also affect reproduction in Mytilus edulis (Myrand et al., 2000).  In shallow lagoons mortality began in late July at the end of a major spawning event when temperatures peaked at >20°C.  These mussels had a low energetic content post spawning and had stopped shell growth.  It is likely that the high temperatures caused mortality due to the reduced condition of the mussels post-spawning (Myrand et al., 2000). Gamete production does not appear to be affected by temperature (Suchanek, 1985).

Power stations have the potential to cause an increase in sea temperature of up to 15°C (Cole et al., 1999), although this impact will be localised.  However, as mussels are of the most damaging biofouling organisms on water outlets of power stations, they are clearly not adversely affected (Whitehouse et al., 1985; Thompson et al., 2000).

Most of the other species within the biotope are eurythermal (e.g. Patella vulgata and Nucella lapillus) and are hardy intertidal species that tolerate long periods of exposure to the air and consequently wide variations in temperature. In addition, most species are distributed to the north of south of the British Isles and unlikely to be adversely affected by long-term temperature changes at the benchmark level. Corallina officinalis, however, experienced severe damage during the unusually hot summer of 1983 (Hawkins & Hartnoll, 1985).

Sensitivity assessment. Based on the wide range of temperature tolerance of Mytilus edulis and its limited effect on its physiology, it is concluded that the acute and chronic changes described by the benchmark would have no effect unless an acute change exceeded thermal tolerances in summer.  Increased temperatures are likely to favour chthamalid barnacles rather than Semibalanus balanoides (Southward et al. 1995). Chthamalus montagui and Chthamalus stellatus are warm water species, with a northern limit of distribution in Britain so are likely to be tolerant of long-term increases in temperature, while Semibalanus balanoides is boreal and at its southern limit the British Isles. Thus, an increase in temperature may lead to a change in the dominant species of barnacle. However, barnacle populations are highly connected, with a good larval supply and high dispersal potential (Wethey et al., 2011, Rognstad et al., 2014). Therefore, larvae are likely to be supplied by local populations to counteract local reproductive failures and resistance is therefore assessed as ‘High’ and resilience as ‘High’ (by default). This biotope is therefore considered to be ‘Not sensitive’ at the pressure benchmark. Sensitivity to longer-term, broad-scale perturbations such as increased temperatures from climate change would, however, be greater, based on the extent of the impact. 

Temperature decrease (local)

Benchmark. A 5°C decrease in temperature for one month, or 2°C for one year. Further detail

Evidence

Many intertidal species are tolerant of freezing conditions as they  are exposed to extremes of low air temperatures during periods of emersion. They must also be able to cope with sharp temperature fluctuations over a short period of time during the tidal cycle. In winter air temperatures are colder than the sea, conversely in summer air temperatures are much warmer than the sea. Species that occur in the intertidal are therefore generally adapted to tolerate a range of temperatures, with the width of the thermal niche positively correlated with the height of the shore that the animal usually occurs at (Davenport & Davenport, 2005).

The barnacle Semibalanus balanoides is primarily a ‘northern’ species with an arctic-boreal distribution. Long-term time series show that recruitment success is correlated to lower sea temperatures (Mieszkowska et al., 2014). Due to warming temperatures its range has been contracting northwards. Temperatures above 10 to 12 ^oC inhibit reproduction (Barnes, 1957, 1963, Crisp & Patel, 1969) and laboratory studies suggest that temperatures at or below 10 ^oC for 4-6 weeks are required in winter for reproduction, although the precise threshold temperatures for reproduction are not clear (Rognstad et al., 2014).

Mytilus edulis is a eurytopic species found in a wide temperature range and in areas which frequently experience freezing conditions and are vulnerable to ice scour (Seed & Suchanek 1992).  After acclimation of individuals of Mytilus edulis to 18°C, Kittner & Riisgaard (2005) observed that the filtrations rates were at their maximum between 8.3 and 20 °C and below this at 6 °C the mussels closed their valves.  However, after being acclimated at 11 °C for five days, the mussels maintained the high filtration rates down to 4 °C.  Hence, given time, mussels can acclimatise and shift their temperature tolerance.  Filtration in Mytilus edulis was observed to continue down to -1 °C, with high absorption efficiencies (53-81 %) (Loo, 1992).

The tolerance of Semibalanus balanoides collected in the winter (and thus acclimated to lower temperatures) to low temperatures was tested in the laboratory. The median lower lethal temperature tolerance was -14.6 ^oC (Davenport & Davenport, 2005) A decrease in temperature at the pressure benchmark is therefore unlikely to negatively affect this species. The same series of experiments indicated that median lower lethal temperature tolerances for Mytilus edulis was -8.2 ^oC . A decrease in temperature at the pressure benchmark is therefore unlikely to negatively affect these species.

Sensitivity assessment. Based on the wide temperature tolerance range of Mytilus edulis and its limited effect on its physiology, it is concluded that the acute and chronic changes described by the benchmark would have limited effect.  Similarly, based on global temperatures and the link between cooler winter temperatures and reproductive success, Semibalanus balanoides is also considered to be unaffected at the pressure benchmark. Based on the characterizing species this biotope is considered to have ‘High’ resistance and ‘High resilience (by default) to this pressure and is therefore considered to be ‘Not sensitive’. 

Salinity increase (local)

Benchmark. A increase in one MNCR salinity category above the usual range of the biotope or habitat. Further detail

Evidence

Local populations may be acclimated to the prevailing salinity regime and may, therefore, exhibit different tolerances to other populations subject to different salinity conditions and therefore, caution should be used when inferring tolerances from populations in different regions.  This biotope is found in full (30-35 ppt) salinity (Connor et al., 2004). Biotopes found in the intertidal will naturally experience fluctuations in salinity where evaporation increases salinity and inputs of rainwater expose individuals to freshwater. Species found in the intertidal are therefore likely to have some form of behavioural or physiological adaptations to changes in salinity. 

Mytilus edulis is found in a wide range of salinities from variable salinity areas (18-35ppt) such as estuaries and intertidal areas, to areas of more constant salinity (30-35ppt) in the sublittoral (Connor et al., 2004).  Furthermore, mussels in rock pools are likely to experience hypersaline conditions on hot days.  Newell (1979) recorded salinities as high as 42 psu in intertidal rock pools, suggesting that Mytilus edulis can tolerate high salinities.  

The associated species are typically found in a range of salinities. Corallina officinalis is found in tide pools where salinities may fluctuate markedly during exposure to the air. Kinne (1971) cites maximal growth rates for Corallina officinalis between 33 and 38 psu in Texan lagoons.  Laboratory experiments have defined the upper and lethal lower limits for Palmaria palmata as 15 psu and 50 psu, (Karsten et al., 2003) with optimal salinity defined as 23-34 psu (Robbins, 1978). 

In the laboratory, Semibalanus balanoides was found to tolerate salinities between 12 and 50 psu (Foster, 1970). Young Littorina littorea inhabit rock pools where salinity may increase above 35psu. Thus, the associated species may be able to tolerate some increase in salinity.  

Sensitivity assessment. Little direct evidence was found to assess sensitivity to this pressure. Although some increases in salinity may be tolerated by the associated species present these are generally short-term and mitigated during tidal inundation.  This biotope is considered, based on the distribution  of Mytilus edulis,  and the associated red algal species on the mid to lower shore to be sensitive to a persistent increase in salinity to > 40 ppt. Resistance is therefore assessed as ‘Low’ and recovery as ‘Medium’ (following restoration of usual salinity). Sensitivity is therefore assessed as ‘Medium'.

Salinity decrease (local)

Benchmark. A decrease in one MNCR salinity category above the usual range of the biotope or habitat. Further detail

Evidence

Mytilus edulis is found in a wide range of salinities from variable salinity areas (18-35 ppt) such as estuaries and intertidal areas, to areas of more constant salinity (30-35ppt) in the sublittoral (Connor et al., 2004).  In addition, Mytilus edulis thrives in brackish lagoons and estuaries, although, this is probably due to the abundance of food in these environments rather than the salinity (Seed & Suchanek, 1992). Mytilus edulis was recorded to grow in a dwarf form in the Baltic sea where the average salinity was 6.5 psu (Riisgård et al., 2013).  Mytilus edulis exhibits a defined behavioural response to reducing salinity, initially only closing its siphons to maintain the salinity of the water in its mantle cavity, which allows some gaseous exchange and therefore maintains aerobic metabolism for longer.  If the salinity continues to fall the valves close tightly (Davenport ,1979; Rankin & Davenport, 1981).  In the long-term (weeks) Mytilus edulis can acclimate to lower salinities (Almada-Villela, 1984; Seed & Suchanek, 1992; Holt et al.,1998).  Almada-Villela (1984) reported that the growth rate of individuals exposed to only 13 psu reduced to almost zero but had recovered to over 80% of control animals within one month.  Observed differences in growth are due to physiological and/or genetic adaptation to salinity.

Decreased salinity has physiological effects on Mytilus edulis; decreasing the heart rate (Bahmet et al., 2005), reducing filtration rates (Riisgård et al., 2013), reducing growth rate (Gruffydd et al., 1984) and reducing the immune function (Bussell et al., 2008).  Both Bahmet et al., (2005); Riisgård et al., (2013) noted that filtration and heart rates return to normal within a number of days acclimation or a return to the original salinity.  However, Riisgard et al., (2013) did observe that mussels from an average of 17 psu found it harder to acclimate between the salinity extremes than those from an average of 6.5 psu.  This observation may mean that mussels in a variable/lower salinity environment are more able to tolerate change than those found at fully marine salinities.  In extreme low salinities, e.g. resulting from storm runoff, large numbers of mussels may be killed (Keith Hiscock pers comm.).  However, Bailey et al., (1996) observed very few mortalities when exposing Mytilus edulis to a range of salinities as low as 0ppt for two weeks at a range of temperatures.  It was also noted that there was a fast recovery rate.

Semibalanus balanoides are tolerant of a wide range of salinity and can survive periodic emersion in freshwater, e.g. from rainfall or freshwater run-off, by closing their opercular valves (Foster, 1971b). They can also withstand large changes in salinity over moderately long periods of time by falling into a "salt sleep".

Similarly, most of the characterizing species (e.g. Littorina littorea and Patella vulgata) are found in a wide range of salinities and are probably tolerant of variable or reduced salinity. The intertidal interstitial invertebrates and epifauna probably experience short-term fluctuating salinities, with reduced salinities due to rainfall and freshwater runoff when emersed. Prolonged reduction in salinity, e.g. from full to reduced due to e.g. freshwater runoff, is likely to reduce the species richness of the biotope due to loss of less tolerant red algae and some intolerant invertebrates. However, the dominant species will probably survive and the integrity of the biotope is likely to be little affected. Areas of freshwater runoff in the intertidal promote the growth of ephemeral greens, probably due to their tolerance of low salinities and inhibition of grazing invertebrates. 

Sensitivity assessment. Based on reported distributions of Mytilus edulis and the results of experiments to assess salinity tolerance thresholds and behavioural and physiological responses in Mytilus edulis and Semibalanus balanoides it is considered that the benchmark decrease in salinity would not result in mortality of the characterizing species in biotopes that were previously fully marine. Resistance is therefore assessed as 'High' and resilience as 'High', based on no effect to recover from and the biotope is considered to be 'Not sensitive'. 

Water flow (tidal current) changes (local)

Benchmark. A change in peak mean spring bed flow velocity of between 0.1 m/s to 0.2 m/s for more than one year. Further detail

Evidence

Mytilus edulis biotopes are recorded from weak (<0.5 m/s) to strong (up to 3 m/s) tidal streams (Connor et al., 2004). Although this specific biotope is found in areas dominated by wave action, dense Semibalanus balanoides and Mytilus edulis populations occur in tidal estuaries in Maine, where peak, tidal flows are >1.1 m/s, (Leonard, et al., 1998) indicating the characterizing species are able to thrive in areas with high flows. 

 Flow rate has been shown to influence the strength and number of byssus threads that are produced by Mytilus edulis and other Mytilus spp. with mussels in areas of higher flow rate demonstrating stronger attachment (Dolmer & Svane, 1994; Alfaro, 2006).  Young (1985) demonstrated that byssus thread production and attachment increased with increasing water agitation. Higher current speed brings food to the bottom layers of the water column, and hence near to the mussels, at a higher rate (Frechette et al., 1989).   Widdows et al., (2002) found that there was no change in filtration rate of Mytilus edulis between 0.05 and 0.8 m/s and that above 0.8 m/s the filtration rate declined mainly because the mussels became detached from the substratum in the experimental flume tank.  Widdows et al., (2002) noted that their results were consistent with field observations, as mussels show preferential settlement and growth in areas of high flow, They also reported that Jenner et al.,(1998; cited in Widdows et al., 2002) observed that biofouling of cooling water systems by mussels was only reduced significantly when mean current speeds reached 1.8-2.2 m/s and that mussels were absent at >2.9 m/s.

Growth and reproduction of Semibalanus balanoides are influenced by food supply and water velocity (Bertness et al., 1991). Laboratory experiments demonstrate that barnacle feeding behaviour alters over different flow rates but that barnacles can feed at a variety of flow speeds (Sanford et al., 1994). The flow tank used velocities of 0.03, 0.07 and 0.2 m/s and a higher proportion of barnacles fed at higher flow rates (Sanford et al., 1994). Feeding was passive, meaning the cirri are held out to the flow to catch particles; active beating of the cirri to generate feeding currents occurs in still water (Crisp & Southward, 1961). Field observations at sites in southern New England (USA) that experience a number of different measured flow speeds, found that barnacles from all sites responded quickly to higher flow speeds, with a higher proportion of individuals feeding when current speeds were higher. Barnacles were present at a range of sites, varying from sheltered sites with lower flow rates (maximum observed flow rates <0.06- 0.1 m/s), a bay site with higher flow rates (maximum observed flows 0.2-0.3 m/s) and open coast sites (maximum observed flows 0.2-0.4 m/s). Recruitment was higher at the site with flow rates of 0.2-0.3 m/s (although this may be influenced by supply) and at higher flow microhabitats within all sites. Both laboratory and field observations indicate that flow is an important factor with effects on feeding, growth and recruitment in Semibalanus balanoides (Sanford et al., 1994, Leonard et al., 1998).

Sensitivity assessment. The biotope is characteristic of extreme to moderate wave exposed conditions where water movement from wave action will greatly exceed the strength of any possible tidal flow. Based on the available evidence the characterizing species Mytilus edulis and Semibalanus balanoides are able to adapt to high flow rates and the biotope is therefore considered to be 'Not sensitive' to an increase in water flow. A decrease in water flow may have some effects on recruitment and growth, but this is not considered to be lethal at the pressure benchmark and resistance is therefore assessed as 'High' and resilience as 'High' by default so that the biotope is considered to be 'Not sensitive'. A decrease in water flow, exceeding the pressure benchmark, coupled with a decrease in wave action, may, however, alter the character of the biotope to LR.MLR.MusF.MytFR or LR.MLR.MusF.MytFves, where brown seaweeds were able to proliferate and the edible periwinkle Littorina littorea was able to colonize.

Emergence regime changes

Benchmark.  1) A change in the time covered or not covered by the sea for a period of ≥1 year or 2) an increase in relative sea level or decrease in high water level for ≥1 year. Further detail

Evidence

Emergence regime is a key factor structuring this (and other) intertidal biotopes.  Increased emergence may reduce habitat suitability for characterizing species through greater exposure to desiccation and reduced feeding opportunities for the mussels and barnacles which feed when immersed.  Semibalanus balanoides is less tolerant of desiccation stress than Chthamalus barnacles species and changes in emergence may, therefore, lead to species replacement and the development of a Chthamalus sp. dominated biotope, more typical of the upper shore may develop. Records suggest that, typically,  above this biotope on the shore there may be a Verrucaria maura zone, and sparse barnacle zone, or a denser barnacle and limpet zone. In addition, patches of the lichen Lichina pygmaea with the barnacle Chthamalus montagui may also occur above this biotope, particularly on southern shores.  Changes in emergence may therefore eventually lead to the replacement of this biotope to one more typical of the upper shore.

Decreased emergence would reduce desiccation stress and allow the attached suspension feeders more feeding time. Predation pressure on mussels and barnacles is likely to increase where these are submerged for longer periods and to prevent colonisation of lower zones. Semibalanus balanoides was able to extend its range into lower zones when protected from predation by the dogwhelk, Nucella lapillus (Connell, 1961). Competition from large fucoids and red algal turfs can also prevent Semibalanus balanoides from extending into lower shore levels (Hawkins, 1983). The biotope is generally found above a zone of either mixed turf-forming red seaweeds), Himanthalia elongata or above the sublittoral fringe kelp Alaria esculenta zone (Connor et al., 2004).  Decreased emergence is likely to lead to the habitat the biotope is found in becoming more suitable for the lower shore species generally found below the biotope, leading to replacement.

The mobile species present within the biotope, including Nucella lapillus, Patella vulgata and the littorinids would be able to relocate to preferred shore levels.

Sensitivity assessment.  Where this biotope occurs on the mid-shore it will be more sensitive to increased emergence whereas lower shore examples may be more sensitive to decreased emergence as the changed conditions occur towards the margins of habitat tolerance.  As emergence is a key factor structuring the distribution of animals on the shore, resistance to a change in emergence (increase or decrease) is assessed as ‘Low’. Recovery is assessed as ‘Medium’, and sensitivity is therefore assessed as 'Medium'.

Wave exposure changes (local)

Benchmark. A change in near shore significant wave height of >3% but <5% for more than one year. Further detail

Evidence

No direct evidence was found to assess the sensitivity of this biotope to changes in wave exposure at the pressure benchmark. This biotope is recorded  from locations that are judged to range from exposed to very exposed (Connor et al., 2004). The natural wave exposure range of this biotope is therefore considered to exceed changes at the pressure benchmark and this biotope is considered to have 'High' resistance and 'High' resilience (by default), to this pressure (at the benchmark). A decrease in wave action,exceeding the pressure benchmark, may however alter the character of the biotope to LR.MLR.MusF.MytFR or LR.MLR.MusF.MytFves, where brown seaweeds were able to proliferate and the edible periwinkle Littorina littorea was able to colonize.

Transition elements & organo-metal contamination

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed but evidence is presented where available.

Contamination at levels greater than the benchmark may impact this biotope. The effects of contaminants on Mytilus edulis species were extensively reviewed by Widdows & Donkin, (1992) and Livingstone & Pipe (1992). Heavy metals were reported to cause sublethal effects and occasionally mortalities in mixed effluents. Barnacles, however, may tolerate fairly high level of heavy metals in nature, for example they possess metal detoxification mechanisms and are found in Dulas Bay, Anglesey, where copper reaches concentrations of 24.5 µg/l, due to acid mine waste (Foster et al., 1978; Rainbow, 1984).

Hydrocarbon & PAH contamination

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed but evidence is presented where available.

Hydrocarbon contamination, at levels greater than the benchmark, e.g. from spills of fresh crude oil or petroleum products, may cause significant loss of component species in the biotope, through impacts on individual species viability or mortality, and resultant effects on the structure of the community (Suchanek, 1993; Raffaelli & Hawkins, 1999).

• The effects of contaminants on Mytilus edulis species were extensively reviewed by Widdows & Donkin, (1992) and Livingstone & Pipe (1992), and summarised in the MarLIN review and Holt et al. (1998). Overall, hydrocarbon tissue burden results in decreased scope for growth and in some circumstances may result in mortalities, reduced abundance or extent of Mytilus edulis (see review).
• Littoral barnacles (e.g. Semibalanus balanoides) have a high resistance to oil (Holt et al., 1995) but may suffer some mortality due to the smothering effects of thick oil (Smith, 1968).
• Gastropods (e.g. Littorina littorea and Patella vulgata) and especially amphipods have been shown to be particularly intolerant of hydrocarbon and oil contamination (see Suchanek, 1993).
• Similarly, laboratory studies of the effects of oil and dispersants on several red algae species (Grandy 1984 cited in Holt et al. 1995) concluded that they were all sensitive to oil/ dispersant mixtures, with little differences between adults, sporelings, diploid or haploid life stages. O'Brien & Dixon (1976) suggested that red algae were the most sensitive group of algae to oil or dispersant contamination.

Synthetic compound contamination

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed but evidence is presented where available.

Synthetic compound contamination, at levels greater than the benchmark, is likely to have a variety of effects depending the specific nature of the contaminant and the species group(s) affected. Barnacles have a low resilience to chemicals such as dispersants, dependant on the concentration and type of chemical involved (Holt et al., 1995). Hoare & Hiscock (1974) reported that the limpet Patella vulgata was excluded from sites within 100-150m of the discharge of acidified, halogenated effluent in Amlwch Bay. Limpets are also extremely intolerance of aromatic solvent based dispersants used in oil spill clean-up. During the clean-up response to the Torrey Canyon oil spill nearly all the limpets were killed in areas close to dispersant spraying. Viscous oil will not be readily drawn in under the edge of the shell by ciliary currents in the mantle cavity, whereas detergent, alone or diluted in sea water, would creep in much more readily and be liable to kill the limpet (Smith, 1968).

Red algae are probably intolerant of chemical contamination. O'Brien & Dixon (1976) suggested that red algae were the most sensitive group of algae to oil contamination, although the filamentous forms were the most sensitive. Laboratory studies of the effects of oil and dispersants on several red algae species, including Palmaria palmata (Grandy, 1984 cited in Holt et al., 1995) concluded that they were all sensitive to oil/ dispersant mixtures, with little differences between adults, sporelings, diploid or haploid life stages. Cole et al. (1999) suggested that herbicides, such as simazina and atrazine were very toxic to macrophytes. In addition, Hoare & Hiscock (1974) noted that almost all red algae were excluded from Amlwch Bay, Anglesey by acidified halogenated effluent discharge.

Radionuclide contamination

Benchmark. An increase in 10µGy/h above background levels. Further detail

Evidence

No evidence.

Introduction of other substances

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed.

De-oxygenation

Benchmark. Exposure to dissolved oxygen concentration of less than or equal to 2 mg/l for one week (a change from WFD poor status to bad status). Further detail

Evidence

 Mytilus edulis is regarded as euryoxic, tolerant of a wide range of oxygen concentrations including zero (Zandee et al., 1986; Wang & Widdows, 1991; Gosling, 1992; Zwaan de & Mathieu, 1992; Diaz & Rosenberg, 1995; Gray et al., 2002). Theede et al., (1969) reported LD50of 35 days for Mytilus edulis exposed to 0.21 mg/l O₂ at 10°C, which was reduced to 25 days with the addition of sulphide (50 mg/l Na₂S.9H₂O).  Jorgensen (1980) observed, by diving, the effects of hypoxia (0.2 -1 mg/l) on benthic macrofauna in marine areas in Sweden over a 3-4 week period.  Mussels were observed to close their shell valves in response to hypoxia and survived for 1-2 weeks before dying (Cole et al., 1999; Jorgensen, 1980). All life stages show high levels of tolerance to low oxygen levels.  Mytilus edulis larvae, for example, are tolerant down to 1.0ml/l, and although the growth of late stage larvae is depressed in hypoxic condition, the settlement behaviour does not seem to be affected (Diaz & Rosenberg 1995).  Based on the available evidence Mytilus edulis are considered to be resistant to periods of hypoxia and anoxia although sub-lethal effects on feeding and growth may be expected.

Semibalanus balanoides can respire anaerobically, so they can tolerate some reduction in oxygen concentration (Newell, 1979). When placed in wet nitrogen, where oxygen stress is maximal and desiccation stress is low, Semibalanus balanoides have a mean survival time of 5 days (Barnes et al., 1963).

Sensitivity assessment. Mytilus edulis is considered to be ‘Not Sensitive’ to de-oxygenation at the pressure benchmark. Resistance is therefore assessed as ‘High’ and resilience as ‘High’ (no effect to recover from), resulting in a sensitivity of 'Not sensitive'.   However, as this biotope occurs in the intertidal, emergence will mitigate the effects of hypoxic surface waters as will the exposure to wave action and water flows and this pressure is considered to be 'Not relevant'.

Nutrient enrichment

Benchmark. Compliance with WFD criteria for good status. Further detail

Evidence

No direct evidence was found to assess this pressure. A slight increase in nutrient levels could be beneficial for barnacles and mussels by promoting the growth of phytoplankton levels and therefore increasing zooplankton levels. Limpets and other grazers would also benefit from increased growth of benthic microalgae. However, Holt et al. (1995) predict that smothering of barnacles or mussels by ephemeral green algae is a possibility under eutrophic conditions.

Sensitivity assessment. The pressure benchmark is set at a level that is relatively protective and based on the evidence and considerations outlined above the biological assemblage, including the clumps of Mytilus edulis, are considered to be 'Not sensitive' at the pressure benchmark. Resistance and resilience are therefore assessed as 'High'.

Organic enrichment

Benchmark. A deposit of 100 gC/m²/yr. Further detail

Evidence

Organic enrichment may lead to eutrophication with adverse environmental effects including deoxygenation, algal blooms and changes in community structure (see nutrient enrichment and de-oxygenation). No evidence was found for piddocks to support the assessment of sensitivity to this pressure. Mytilus edulis, however, has been found to be generally insensitive to an increase in organic matter resulting from human activities. Mytilus edulis has been recorded in areas around sewage outflows (Akaishi et al. 2007; Lindahl & Kollberg, 2008; Nenonen et al. 2008; Giltrap et al. 2013) suggesting that they are highly tolerant of the increase in organic material that would occur in these areas.  A number of studies have also highlighted the ability of Mytilus edulis to utilise the increased volume of organic material available at locations around salmon farms.  Reid et al. (2010) noted that Mytilus edulis could absorb organic waste products from a salmon farm with great efficiency.  Increased shell length, wet meat weight, and condition index were shown at locations within 200m from a farm in the Bay of Fundy allowing a reduced time to market (Lander et al., 2012). It has been shown that regardless of the concentration of organic matter Mytilus edulis will maintain its feeding rate by compensating with changes to filtration rate, clearance rates, production of pseudofaeces and absorption efficiencies (Tracey, 1988; Bayne et al., 1993; Hawkins et al., 1996).  

The biotope occurs in tide-swept or wave exposed areas (Connor et al., 2004) preventing a build-up of organic matter so that the biotope is considered to have a low risk of organic enrichment at the pressure benchmark.

Sensitivity assessment. Based on the observation of Mytilus edulis thriving in areas of increased organic matter (Lander et al., 2012, Reid et al., 2010), it was assumed that Mytilus edulis clumps have a ’High’ resistance to increased organic matter at the pressure benchmark.  Resilience is therefore assessed as ‘High’ (no effect to recover from).  No evidence was found to support an assessment for Semibalanus balanoides.  As organic matter particles in suspension could potentially be utilised as a food resource or consumed by Mytilus edulis and other species present within the biotope with excess likely to be rapidly removed by wave action or coverall resistance of the biological assemblage within the biotope is assessed as 'High' and resilience as 'High' so that this biotope is assessed as 'Not sensitive'.

Physical loss (to land or freshwater habitat)

Benchmark. A permanent loss of existing saline habitat within the site. Further detail

Evidence

All marine habitats and benthic species are considered to have a resistance of ‘None’ to this pressure and to be unable to recover from a permanent loss of habitat (resilience is ‘Very Low’).  Sensitivity within the direct spatial footprint of this pressure is therefore ‘High’.  Although no specific evidence is described confidence in this assessment is ‘High’, due to the incontrovertible nature of this pressure.

Physical change (to another seabed type)

Benchmark. Permanent change from sedimentary or soft rock substrata to hard rock or artificial substrata or vice-versa. Further detail

Evidence

This biotope is characterized by the hard rock substratum to which barnacles and mussels can firmly attach. A change to a sedimentary substratum would significantly alter the character of the biotope. The biotope is, therefore, considered to have None resistance to this pressure, resilience is Very low (the pressure is a permanent change) and sensitivity is assessed as High.

Physical change (to another sediment type)

Benchmark. Permanent change in one Folk class (based on UK SeaMap simplified classification). Further detail

Evidence

Not relevant to biotopes occurring on bedrock.

Habitat structure changes - removal of substratum (extraction)

Benchmark. The extraction of substratum to 30 cm (where substratum includes sediments and soft rock but excludes hard bedrock). Further detail

Evidence

The species characterizing this biotope are epifauna or epiflora occurring on rock and would be sensitive to the removal of the habitat. However, extraction of rock substratum is considered unlikely and this pressure is considered to be ‘Not relevant’ to hard substratum habitats.

Abrasion / disturbance of the surface of the substratum or seabed

Benchmark. Damage to surface features (e.g. species and physical structures within the habitat). Further detail

Evidence

The species characterizing this biotope, barnacles, mussels and attached red seaweeds are all attached and occur on the surface. They therefore have no protection from abrasion and can be damaged or killed or displaced. Displaced mussels may be able to reattach using byssus threads but barnacles have no mechanisms for reattachmnet if they survived removal. The level of effect will depend on the magnitude, extent and duration of the pressure.

The effects of trampling (a source of abrasion) on barnacles appears to be variable with some studies not detecting significant differences between trampled and controlled areas (Tyler-Walters & Arnold, 2008). However, this variability may be related to differences in trampling intensities and abundance of populations studied. The worst case incidence was reported by Brosnan and Crumrine (1994) who reported that a trampling pressure of 250 steps in a 20x20 cm plot one day a month for a period of a year significantly reduced barnacle cover at two study sites. Barnacle cover reduced from 66% to 7% cover in 4 months at one site and from 21% to 5% within 6 months at the second site. Overall barnacles were crushed and removed by trampling. Barnacle cover remained low until recruitment the following spring. Long et al. (2011) also found that heavy trampling (70 humans km^-1 shoreline h^-1) led to reductions in barnacle cover. 

 Activities resulting in abrasion and disturbance can either directly affect the mussel by crushing them, or indirectly affect them by the weakening or breaking of their byssus threads making them vulnerable to displacement (Denny, 1987) where they are unlikely to survive (Dare, 1976).  In addition, abrasion and sub-surface damage may attract mobile scavengers and predators including fish, crabs, and starfish to feed on exposed, dead and damaged individuals and discards (Kaiser & Spencer, 1994; Ramsay et al., 1998; Groenewold & Fonds, 2000; Bergmann et al., 2002).  This effect will increase predation pressure on surviving damaged and intact Mytilus edulis when submerged.  A number of activities or events that result in abrasion  and disturbance and their impacts on mussel beds are described below, based on the review by Mainwaring et al. (2014).

Large declines of the Mytilus californianus from mussel beds due to trampling have been reported (Brosnan, 1993; Brosnan & Crumrine, 1994; Smith & Murray, 2005).  Brosnan & Crumrine (1994) recorded the loss of 54% of mussels from a single experimental plot on one day.  Mussels continued to be lost throughout the experimental period, forming empty patches larger than the experimental plots.  The empty patches continued to expand after trampling had ceased, due to wave action.  Brosnan (1993) also reported a 40% loss of mussels from mussel beds after three months of trampling, and a 50% loss within a year.  Van de Werfhorst & Pearse (2007) examined Mytilus californianus abundance at sites with differing levels of trampling disturbance.  The highest percentage of mussel cover was found at the undisturbed site while the severely disturbed site showed low mussel cover. Brosnan and Crumrine (1994) noted that mussels that occupied hard substrata but did not form beds were also adversely affected.  Although only at low abundance (2.5% cover), all mussels were removed by trampling within 4 months.  Brosnan & Crumrine (1994) noted that mussels were not common and confined to crevices in heavily trampled sites.  Similarly, the mussel bed infauna (e.g. barnacles) was adversely affected, and were crushed or lost with the mussels to which they were attached.  However, Beauchamp & Gowing (1982) did not observe any differences in mussel density between sites that differed in visitor use.

Collision of objects such as wave driven logs (or similar flotsam), is known to cause removal of patches of mussels from mussel beds (Seed & Suchanek, 1992; Holt et al., 1998).  When patches occur in mussel beds a good recruitment could result in a rapid recovery or the patch may increase in size through weakening of the byssus threads of the remaining mussels leaving them vulnerable to erosion from storm damage (Denny, 1987). Damage in areas of high wave exposure is likely to result in increased erosion and a patchy distribution although recruitment may be high.  In sheltered areas damage may take a lot longer due to limited larval supply, although the frequency of destruction through wave driven logs would be less than in high wave exposure.  Similar effects could be observed through the grounding of a vessel, the dropping of an anchor or the laying of a cable, although the scale of damage clearly differs.Shifting sand is known to limit the range of Mytilus edulis through burial and abrasion (Daly & Mathieson, 1977).

Various fishing methods also result in abrasion of the mussel beds.  Bait collection through raking will cause surface abrasion and the removal of patches of mussel resulting in the damage and recovery times described above.  Holt et al., (1998) reported that hand collection, or using simple hand tools occurs in small artisanal fisheries.  They suggested that moderate levels of collection by experienced fishermen may not adversely affect the biodiversity of the bed.  But they also noted that even artisanal hand fisheries can deplete the mussel biomass on accessible beds in the absence of adequate recruitment of mussels. Smith & Murray (2005) observed a significant decrease in mussel mass (g/m²), density (no./m²), percentage cover and mean shell length due to low-intensity simulated bait-removal treatments (2 mussels / month) for 12 months (Smith & Murray, 2005).  They also stated that the initial effects of removal were ‘overshadowed’ by loss of additional mussels during time periods between treatments, probably due to the indirect effect of weakening of byssal threads attachments between the mussel leaving them more susceptible to wave action (Smith & Murray, 2005).  The low-intensity simulated bait-removal treatments had reduced percentage cover by 57.5% at the end of the 12 month experimental period.  Smith & Murray (2005) suggested that the losses occurred from collection and trampling are far greater than those that occur by natural causes.  This conclusion was reached due to significant results being displayed for human impact despite the experiment taking place during a time of high natural disturbance from El Niño–Southern Oscillation (ENSO).

Sensitivity assessment. Surface abrasion may remove mussel clumps and algae and Semibalanus balanoides. Resistance is therefore assessed as ‘Low’ for mussels, barnacles and algae. All components are predicted to remover within 2 -10 years, so that resilience is considered to be ‘Medium’ and sensitivity is ‘Medium’.   

Penetration or disturbance of the substratum subsurface

Benchmark. Damage to sub-surface features (e.g. species and physical structures within the habitat). Further detail

Evidence

The species characterizing this biotope group are epifauna or epiflora occurring on rock which is resistant to subsurface penetration.  The assessment for the abrasion pressure is therefore considered to equally represent sensitivity to this pressure.

Changes in suspended solids (water clarity)

Benchmark. A change in one rank on the WFD (Water Framework Directive) scale e.g. from clear to intermediate for one year. Further detail

Evidence

In general, increased suspended particles may enhance food supply (where these are organic in origin) or decrease feeding efficiency (where the particles are inorganic and require greater filtration efforts).  Very high levels of silt may clog respiratory and feeding organs of the suspension feeding Semibalanus balanoides and Mytilus edulis. In addition, increased turbidity will decrease light penetration reducing photosynthesis by macroalgae within this biotope.  Increased levels of particles may increase scour and deposition in the biotope depending on local hydrodynamic conditions, although changes in substratum are assessed through the physical change (to another seabed type) pressure.

A significant decrease in suspended organic particles may reduce food input to the biotope resulting in reduced growth and fecundity of suspension feeding barnacles and mussels. However, local primary productivity may be enhanced where suspended sediments decrease, increasing food supply.  Decreased suspended sediment may increase macroalgal competition enhancing diversity but is considered unlikely to significantly change the character of the biotope as colonisation by larger brown macroalgae is limited by the friability of the surface which is unsuitable for attachment.

Macroalgae within the biotope may be sensitive to decreased light penetration, however Hily et al. (1992) found that, in conditions of high turbidity, the characterizing species Ceramium virgatum (as Ceramium rubrum) dominated sediments in the Bay of Brest, France. It is most likely that Ceramium virgatum thrived because other species of algae could not. Whilst the field observations in the Bay of Brest suggested that an increase in abundance of Ceramium virgatum might be expected in conditions of increased turbidity, populations where light becomes limiting will be adversely affected. However, in shallow depths and the intertidal, photosynthesis can occur during low tides (as long as sediments are not deposited) and Ceramium virgatum may benefit from increased turbidity through decreased competition. The other  red algae species found within this biotope are considered to have similar tolerances based on tolerance of shade and/or eutrophic conditions.

Mytilus edulis are often found in areas with high levels of turbidity.  For example, the average suspended particulate matter (SPM) concentration at Hastings Shingle Bank was 15 -20 mg/l in June 2005, reaching 50 mg/l in windier (force 4) conditions, although a concentration of 200 mg/l was recorded at this site during gales (Last et al., 2011). It may be possible for Mytilus edulis to adapt to a permanent increase in SPM by decreasing their gill size and increasing their palp size in areas of high turbidity (Theisen, 1982; Essink, 1999).  In areas of variable SPM it is likely that the gill size would remain the same but the palp would adapt (Essink, 1999).  Whilst the ability to adapt may prevent immediate declines in health, the energetic costs of these adaptations may result in reduced fitness; the extent of which is still to be established.  Concentrations above 250 mg/l have been shown to impair the growth of filter-feeding organisms (Essink, 1999).  But Purchon (1937) found that concentrations of particulates as high a 440 mg/l did not affect Mytilus edulis and that mortality was only occurred when mud was added to the experiment bringing the concentrations up to 1220 mg/l.  The reason for some of the discrepancy between studies may be due to the volume of water used in the experiment.  Loosanoff (1962) found that in small quantities of turbid water (due to particulates) the mussel can filter out all of the particulates within a few minutes whereas in volumes >50 gallons per individual the mussel becomes exhausted before the turbidity has been significantly lowered, causing it to close its shell and die. Based on a comprehensive literature review, Moore (1977) concluded that Mytilus edulis displayed a higher tolerance to high SPM concentrations than many other bivalves although the upper limit of this tolerance was not certain.  He also hypothesised that the ability of the mussel to clean its shell in such conditions played a vital role in its success along with its pseudofaecal expulsion.

Mytilus edulis may be more sensitive to decreased turbidity where this reflects a decrease in the availability of organic matter and seston. Winter (1972) (cited by Moore, 1977) recorded 75% mortality of Mytilus edulis in concentrations of 1.84-7.36 mg/l when food was also available.   However, a relatively small increase in SPM concentration e.g. from 10 mg/l to 90 mg/l was found to increase growth rates (Hawkins et al., 1996). 

Gyory et al., (2013) found that increased turbidity triggered the release of larvae by Semibalanus balanoides, a response which may allow larval release to be timed with high levels of phytoplankton and at times where predation on larvae may be lowered due to the concentration of particles. Storm events that stir up sediments are also associated with larval release (Gyory & Pineda, 2011).

Sensitivity assessment.  Evidence indicates that Mytilus edulis can tolerate a broad range of suspended solids.  The benchmark for this pressure refers to a change in turbidity of one rank on the Water Framework Directive (WFD) scale.  Mussel beds form in relatively clear waters of open coasts and wave exposed shores and on sediments in sheltered coast (where turbulent water flow over the mussel beds could resuspend sediments locally) and in turbid bays and estuaries.  Therefore, is unlikely that a change in turbidity by of one rank (e.g. from 300 to 100 mg/l or <10 to 100 mg/l) will significantly affect the Mytilus edulis within this biotope.   Resistance to this pressure is therefore assessed as ‘High.  Recovery is assessed ‘High’ (no impact to recover from), and sensitivity is therefore 'Not sensitive'.  The biotope is therefore considered to be ‘Not sensitive’.  An indirect effect of increased turbidity and reduced light penetration may be reduced phytoplankton productivity which could reduce the food availability for suspension feeders.  However, as Mytilus edulis use a variety of food sources and food is brought in from other areas with currents and tides, the effect is likely to be minimal.  This species and the biotopes it forms are therefore not sensitive to changes in water clarity.

Smothering and siltation rate changes (light)

Benchmark. ‘Light’ deposition of up to 5 cm of fine material added to the seabed in a single discrete event. Further detail

Evidence

Barnacle feeding may be affected however, wave action on rocky shores is likely to rapidly mobilise and remove deposits alleviating the effect of smothering. Barnacles have planktonic larvae so can recolonise affected area so recovery should be high (Hill, 2000). However, the lower limits of Semibalanus balanoides (as Balanus balanoides) appear to be set by levels of sand inundation on sand-affected rocky shores in New Hamshire (Daly & Mathieson, 1977).

Mytilus edulis occurs in areas of high suspended particulate matter (SPM) and therefore a level of siltation is expected from the settling of SPM.  In addition, the high rate of faecal and pseudofaecal matter production by the mussels naturally results in siltation of the seabed, often resulting in the formation of large mounds beneath the mussel bed.  For example, at Morecambe Bay an accumulation of mussel-mud (faeces, pseudofaeces and washed sand) of 0.4-0.5 m between May 1968 and September 1971 resulted in the mortality of young mussels (Daly & Mathieson, 1977).  In order to survive the mussels needed to keep moving upwards to stay on the surface.  Many individuals did not make it to the surface and were smothered by the accumulation of mussel-mud (Daly & Mathieson, 1977), so that whilst Mytilus edulis does have the capacity to vertically migrate through sediment some individuals will not survive. 

Sand burial has been shown to determine the lower limit of Mytilus edulis beds (Daly & Mathieson, 1977).  Burial of Mytilus edulis beds by large scale movements of sand, and resultant mortalities have been reported from Morecambe Bay, the Cumbrian coast and Solway Firth (Holt et al., 1998).  Essink (1999) recorded fatal burial depths of 1-2 cm for Mytilus edulis and suggested that they had a low tolerance of sedimentation based on investigations by R.Bijkerk (cited by Essink, 1999).  Essink (1999) suggested that deposition of sediment (mud or sand) on shallow mussel beds should be avoided.  However, Widdows et al. (2002) noted that mussels buried by 6 cm of sandy sediment (caused by resuspension of sediment due to turbulent flow across the bed) were able to move to the surface within one day.  Conversely, Condie (2009) (cited by Last et al., 2011) reported that Mytilus edulis was tolerant of repeated burial events.

Last et al., (2011) carried out burial experiments on Mytilus edulis in pVORTs.  They used a range of burial depths and sediment fractions and temperatures.  It was found that individual mussels were able to survive burial in depths of 2, 5 and 7 cm for over 32 days although the deeper and longer the mussels were buried the higher the mortality.  Only 16% of buried mussels died after 16 days compared to almost 50% mortality at 32 days.  Mortality also increased sharply with a decrease in particle size and with increases in temperature from 8.0 and 14.5 to 20 °C.  The ability of a proportion of individuals to emerge from burial was again demonstrated with approximately one quarter of the individuals buried at 2 cm resurfacing.  However, at depths of 5 cm and 7 cm no emergence was recorded (Last et al., 2011).  The lower mortality when buried in coarse sands may be related to the greater number of individuals who were able to emerge in these conditions and emergence was to be significant for survival.

It is unclear whether the same results would be recorded when mussels are joined by byssal threads or whether this would have an impact on survival (Last et al., 2011), although Daly & Mathieson (1977) recorded loose attachments between juvenile mussels during a burial event and some of these were able to surface.  It was not clear whether the same ability would be shown by adult mussels in a more densely packed bed.

Sensitivity  assessment. Semibalanus balanoides is found permanently attached to hard substrates and is a suspension feeder. This species, therefore, has no ability to escape from silty sediments which would bury individuals and prevent feeding and respiration.  The inability of Mytilus edulis to emerge from sediment deeper than 2 cm (Last et al., 2011, Essink, 1999, Daly & Matthieson, 1977) and the increased  mortality with depth and reduced particle size observed by Last et al. (2011) suggest that some mussels may die if smothering is prolonged and resistance is assessed as 'Medium' for both Mytilus edulis and Semibalanus balanoides.   Resilience is assessed as ‘High’ (recovery within 2 years) and sensitivity is, therefore, assessed as ‘Low’.  Survival will be higher in winter months when temperatures are lower and physiological demands are decreased.  It should be noted that the level of exposure may be reduced by wave action or water flows so that site-specific vulnerability will be negligible where sediments do not accumulate.

Smothering and siltation rate changes (heavy)

Benchmark. ‘Heavy’ deposition of up to 30 cm of fine material added to the seabed in a single discrete event. Further detail

Evidence

Barnacle feeding may be affected however by smothering, wave action on rocky shores is likely to rapidly mobilise and remove deposits alleviating the effect of smothering. However, the lower limits of Semibalanus balanoides (as Balanus balanoides) appear to be set by levels of sand inundation on sand-affected rocky shores in New Hamshire (Daly & Mathieson, 1977).Sand burial has been shown to determine the lower limit of Mytilus edulis beds (Daly & Mathieson, 1977a).  Burial of Mytilus edulis beds by large scale movements of sand, and resultant mortalities have been reported from Morecambe Bay, the Cumbrian coast and Solway Firth (Holt et al., 1998).  Essink (1999) recorded fatal burial depths of 1-2 cm for Mytilus edulis and suggested that Mytilus edulis a low tolerance of sedimentation based on investigations by R.Bijkerk (cited by Essink, 1999).  However, Widdows et al. (2002) noted that mussels buried by 6 cm of sandy sediment (caused by resuspension of sediment due to turbulent flow across the bed) were able to move to the surface within one day. 

Last et al., (2011) carried out a series of burial experiments on Mytilus edulis in pVORTs using a range of burial depths, sediment fractions and temperatures.  It was found that individual mussels were able to survive burial in depths of 2, 5 and 7cm for over 32 days although the deeper and longer the mussels were buried the higher the mortality.  Only 16% of buried mussels died after 16 days compared to almost 50% mortality at 32 days.  Mortality also increased sharply with a decrease in particle size and with increases in temperature from 8.0 and 14.5 to 20°C.  The ability of a proportion of individuals to emerge from burial was again demonstrated, with approximately one quarter of the individuals buried at 2cm resurfacing.  However, at depths of 5 cm and 7cm no emergence was recorded (Last et al., 2011).  The lower mortality when buried in coarse sands may be related to the greater number of individuals who were able to emerge in these conditions.It is unclear whether the same results would be recorded when mussels are joined by byssal threads or whether this would have an impact on survival (Last et al., 2011), although Daly & Mathieson (1977) recorded loose attachments between juvenile mussels during a burial event and some of these were able to surface.  

Sensitivity assessment. Sensitivity to this pressure will be mediated by site-specific hydrodynamic conditions and the footprint of the impact. Where a large area is covered sediments may be shifted by wave and tides rather than removed. The inability of Mytilus edulis to emerge from sediment deeper than 2 cm (Last et al., 2011, Essink, 1999, Daly & Matthieson, 1977) and the increased mortality with depth and reduced particle size observed by Last et al. (2011) indicates that there may be significant mortality of mussels where sediments persist. Resistance to siltation is therefore assessed as ‘Low’ for Mytilus edulis and Semibalanus balanoides and resilience is assessed as ‘Medium’ (2-10 years).  Survival will be higher in winter months when temperatures are lower and physiological demands are decreased.  However, mortality will depend on the duration of smothering, where wave action rapidly mobilises and removes fine sediments, survival will be muich greater.

Litter

Benchmark. The introduction of man-made objects able to cause physical harm (surface, water column, seafloor or strandline). Further detail

Evidence

Thompson et al., (2004) demonstrated that Semibalanus balanoides, kept in aquaria, ingested microplastics within a few days. However, the effects of the microplastics on the health of exposed individuals have not been identified. Mytilus edulis also ingest microplastics. A laboratory experiment using microbeads of polystyrene, demonstrated uptake of particles by Mytilus edulis within 12 hours (Browne  et al., 2008). After three days some of the the beads were translocated to the circulatory system. Microplastics were excreted in fecal pellets but were still present in hemolymph 48 days later. No toxicological effects were observed and there were no changes in filter feeding activity (Browne et al., 2008). As exposure was short-term it is not clear whether lethal or sub-lethal effects would occur in wild populations over extended periods. There is currently no evidence to assess the level of impact. 

Electromagnetic changes

Benchmark. A local electric field of 1 V/m or a local magnetic field of 10 µT. Further detail

Evidence

No evidence.

Underwater noise changes

Benchmark. MSFD indicator levels (SEL or peak SPL) exceeded for 20% of days in a calendar year. Further detail

Evidence

Not relevant. Wave action on exposed shores is likely to generate high levels of underwater noise. Other sources are not considered likely to result in effects on the biotope.

Introduction of light or shading

Benchmark. A change in incident light via anthropogenic means. Further detail

Evidence

Semibalanus balanides sheltered from the sun grew bigger than unshaded individuals (Hatton, 1938; cited in Wethey, 1984), although the effect may be due to indirect cooling effects rather than shading. Barnacles are also frequently found under algal canopies suggesting that they are tolerant of shading. Light levels have also been demonstrated to influence a number of phases of the reproductive cycle in Semibalanus balanoides.  In general, light inhibits aspects of the breeding cycle. Penis development is inhibited by light (Barnes & Stone, 1972) while Tighe-Ford (1967) showed that constant light inhibited gonad maturation and fertilization. Davenport & Crisp (unpublished data from Menai Bridge, Wales, cited from Davenport et al., 2005) found that experimental exposure to either constant darkness or 6-hour light: 18-hour dark photoperiods induced autumn breeding in Semibalanus. They also confirmed that very low continuous light intensities (little more than starlight) inhibited breeding. Latitudinal variations in the timing of the onset of reproductive phases (egg mass hardening) have been linked to the length of darkness (night) experienced by individuals rather than temperature (Davenport et al., 2005). Changes in light levels associated with climate change (increased cloud cover) were considered to have the potential to alter the timing of reproduction (Davenport et al., 2005) and to shift the range limits of this species southward. However, it is not clear how these findings may reflect changes in light levels from artificial sources, and whether observable changes would occur at the population level as a result. There is, therefore, 'insufficient evidence' on which to base an assessment. 

Barrier to species movement

Benchmark. A permanent or temporary barrier to species movement over ≥50% of water body width or a 10% change in tidal excursion. Further detail

Evidence

No direct evidence was found to assess this pressure. As the larvae of mytilus edulis and Semibalanus balanoides are planktonic and are transported by water movements, barriers that reduce the degree of tidal excursion may alter larval supply to suitable habitats from source populations. However the presence of barriers may enhance local population supply by preventing the loss of larvae from enclosed habitats.  As both species are widely distributed and have larvae capable of long distance transport, resistance to this pressure is assessed as 'High' and resilience as 'High' by default. This biotope is therefore considered to be 'Not sensitive'. 

Death or injury by collision

Benchmark. Injury or mortality from collisions of biota with both static or moving structures due to 0.1% of tidal volume on an average tide, passing through an artificial structure. Further detail

Evidence

Not relevant’ to seabed habitats.  NB. Collision by grounding vessels is addressed under ‘surface abrasion. 

Visual disturbance

Benchmark. The daily duration of transient visual cues exceeds 10% of the period of site occupancy by the feature. Further detail

Evidence

Not relevant.

Genetic modification & translocation of indigenous species

Benchmark. Translocation of indigenous species or the introduction of genetically modified or genetically different populations of indigenous species that may result in changes in the genetic structure of local populations, hybridization, or change in community structure. Further detail

Evidence

This pressure is only relevant to the patches of Mytilus edulis as other species within the biotope are not subject to translocation or cultivation. Commercial cultivation of Mytilus edulis involves the collection of juvenile mussel ‘seed’ or spat (newly settled juveniles ca 1-2cm in length) from wild populations, with subsequent transportation around the UK for re-laying in suitable habitats. As the seed is harvested from wild populations from various locations the gene pool will not necessarily be decreased by translocations.  Movement of mussel seed has the potential to transport pathogens and non-native species (see relevant pressure sections). This pressure assessment is based on Mainwaring et al. (2014) and considers the potential impacts on natural mussel beds of genetic flow between translocated stocks and wild mussel beds.

Two species of Mytilus occur in the UK, Mytilus edulis and Mytilus galloprovincialis.  Mytilus edulis appears to maintain genetic homogeneity throughout its range whereas Mytilus galloprovincialis can be genetically subdivided into a Mediterranean group and an Atlantic group (Beaumont et al. 2007).  Mytilus edulis and Mytilus galloprovincialis have the ability to hybridise in areas where their distribution overlaps e.g. around the Atlantic and European coast (Gardner, 1996; Daguin et al., 2001; Bierne et al., 2002; Beaumont et al., 2004).  In the UK overlaps occur on the North East coast, North East Scotland, South West England and in the North, West and South of Ireland (Beaumont et al., 2007).  It is difficult to identify Mytilus edulis, Mytilus galloprovincialis or hybrids based on shell shape because of the extreme plasticity of shape exhibited by mussels under environmental variation, and a genetic test is required (Beaumont et al., 2007).  There is some discussion questioning the distinction between the two species as the hybrids are fertile (Beaumont et al., 2007).  Hybrids reproduce and spawn at a similar time to both Mytilus edulis and Mytilus galloprovincialis which supports genetic flow between the taxa (Doherty et al., 2009).

There is some evidence that hybrid larvae have a faster growth rate to metamorphosis than pure individuals which may leave pure individuals more vulnerable to predation (Beaumont et al., 1993).  As the physiology of both the hybrid and pure Mytilus edulis is so similar there is likely to be very little impact on the tolerance of the bed to pressures nor a change in the associated fauna.

A review by Svåsand et al. (2007) concluded that there was a lack of evidence distinguishing between different populations to accurately assess the impacts of hybridisation and in particular how the gene flow may be affected by aquaculture.  Therefore, it cannot be confirmed whether farming will have an impact on the genetics of this species beyond a potential for increased hybridisation.

Sensitivity assessment. No direct evidence was found regarding the potential for negative impacts of translocated mussel seed on wild Mytilus edulis populations.  While it is possible that translocation of mussel seed could lead to genetic flow between cultivated beds and local wild populations, there is currently no evidence to assess the impact (Svåsand et al., 2007).  Hybrids would perform the same ecological functions as Mytilus edulis so that any impact relates to the genetic integrity of a bed alone.  This impact is considered to apply to all mussel biotopes equally, as the main habitat-forming species Mytilus edulis is translocated.  Also, given the uncertainty in the identification of the species, habitats or biotopes that are considered to be characterized by Mytilus edulis may in fact contain Mytilus galloprovincialis, their hybrids or a mosaic of the three. Presently, there is no evidence of impact resulting from genetic modification and translocation on Mytilus edulis beds in general or the clumps that characterize this biotope.  

Introduction or spread of invasive non-indigenous species

Benchmark. The introduction of one or more invasive non-indigenous species (INIS). Further detail

Evidence

The carpet sea squirt Didemnum vexillum (syn. Didemnum vestitum; Didemnum vestum) is a colonial ascidian with rapidly expanding populations that have invaded most temperate coastal regions around the world (Kleeman, 2009; Stefaniak et al., 2012; Tillin et al., 2020). It is an ‘ecosystem engineer’ that can change or modify invaded habitats and alter biodiversity (Griffith et al., 2009; Mercer et al., 2009). Didemnum vexillum has colonized and established populations in the northeast Pacific, Canadian and USA coast; New Zealand; France, Spain, and the Wadden Sea, Netherlands; the Mediterranean Sea and Adriatic Sea (Bullard et al., 2007; Coutts & Forrest, 2007; Dijkstra et al., 2007; Valentine et al., 2007a; Valentine et al., 2007b; Lambert, 2009; Hitchin, 2012; Tagliapietra et al., 2012; Gittenberger et al., 2015; Vercaemer et al., 2015; Mckenzie et al., 2017; Cinar & Ozgul, 2023; Holt, 2024). In the UK, Didemnum vexillum has colonized Holyhead marina and Milford Haven, Wales; the west coast of Scotland (marinas around Largs, Clyde, Loch Creran and Loch Fyne), South Devon (Plymouth, Yealm, and Dartmouth estuaries), the Solent, northern Kent, Essex, and Suffolk coasts (Griffith et al., 2009; Lambert, 2009; Hitchin, 2012; Michin & Nunn, 2013; Bishop et al., 2015; Mckenzie et al., 2017; Tillin et al., 2020, Holt, 2024; NBN, 2024).

Although a widespread invader, Didemnum vexillum has a limited ability for natural dispersal since the pelagic larvae remain in the water column for a short time (up to 36 hours). Therefore, it has a short dispersal phase that can allow the species to build localized populations (Herborg et al., 2009; Vercaemer et al., 2015; Holt, 2024). However, Bullard et al. (2007) suggested that Didemnum vexillum can form new colonies asexually by fragmentation. Colonies can produce long tendrils from an encrusting colony, which can fragment, disperse and settle, attaching to suitable hard substrata elsewhere (Bullard et al., 2007; Lambert, 2009; Stefaniak & Whitlatch, 2014). A fragmented colony can spread naturally for up to three weeks transported by ocean currents, attached to floating seaweed, seagrass or other floating biota, or as free-floating spherical colonies (Bullard et al., 2007; Lengyel et al., 2009; Stefaniak & Whitlatch, 2014; Holt, 2024). Fragments can reattach to suitable substrata within six hours of contact. Fragments have the potential to disperse around 20 km before reattachment (Lengyel et al., 2009). Valentine et al. (2007a) reported that colonies of Didemnum vexillum enlarged by 6 to 11 times by asexual budding after 15 days and enlarged 11 to 19 times after 30 days. Valentine et al. (2007a) concluded fragments could successfully grow, survive, and help to spread Didemnum vexillum.

While natural fragmentation of tendrils is thought to allow Didemnum vexillum to invade longer distances and increase its dispersal potential, Stefaniak & Whitlatch (2014) found that only one tendril out of 80 reattached to the flat, bare substrata used in their study, because tendrils required an extensive (at least eight hour) period of contact to reattach. Stefaniak & Whitlatch (2014) suggested that once fragmented from a colony, the success of tendril reattachment was limited, and reattachment was not a major contributor to the invasive success of Didemnum vexillum. However, Stefaniak & Whitlatch (2014) also found that larvae-packed tendril fragments may increase natural dispersal distance, reproduction, and invasive success of Didemnum vexillum, and increase the distance larvae can travel. Not all colonies produce tendrils at all locations.

Human-meditated transport via aquaculture facilities, boat hulls, commercial fishing vessels, and ballast water is probably the most important vector that has aided the long-distance dispersal of Didemnum vexillum and explains its prevalence in harbours and marinas (Bullard et al., 2007; Dijkstra et al., 2007; Griffith et al., 2009; Herborg et al., 2009). Fragmentation of colonies during transport or human disturbance (such as trawling or dredging) could indirectly disperse the species and enable it to find suitable conditions for establishment (Herborg et al., 2009). For example, in oyster farms in British Columbia, large fragments of Didemnum sp. come off oyster strings when they are pulled out of water and other fragments can be pulled off oysters and mussels and thrown back into the water, which is likely to aid dispersal of the invasive species (Bullard et al., 2007). Dijkstra et al. (2007) hypothesised that Didemnum sp. was introduced to the Gulf of Maine with oyster aquaculture in the Damariscotta River and transported via Pacific oysters.

Didemnum vexillum was likely introduced into the UK from northern Europe or Ireland via poorly maintained or not antifouled vessels, movement of contaminated shellfish stock and aquaculture equipment, or via marine industries such as oil, gas, renewables, and dredging (Holt, 2024). Recent evidence from genetic material suggests that human-mediated dispersal, between marinas and shellfish culture sites, is the most likely pathway for connectivity of Didemnum vexillum populations throughout Ireland and Britain (Prentice et al., 2021; Holt, 2024). Didemnum vexillum can disperse away from artificial substrata, invading and colonizing natural substrata in surrounding areas (Tillin et al., 2020). Holt (2024) noted that Didemnum vexillum had not spread as far as feared in the UK since it was first recorded. The current evidence of Didemnum vexillum’s ability to spread on natural habitats in this area is sparse and often conflicting, complicated by genetics and its apparent variable habitat preferences and tolerances and its variable ability to adapt to ‘new’ conditions (Holt 2024).

Didemnum vexillum has a seasonal growth cycle influenced by temperature (Valentine et al., 2007a). Colonies may form large and well-developed encrusting mats in warmer months (June and July). Populations experience more rapid growth from July to September sometimes continuing into December. Colonies begin to decline in health and ‘die-off’ when temperatures drop below 5°C during winter months from around October to April (Gittenberger, 2007; Valentine et al., 2007a; Herborg et al., 2009). Cold water months cause colonies to regress and reduce in size, yet they often regenerate as temperatures warm (Griffith et al., 2009; Kleeman, 2009, Mercer et al., 2009), although some populations may not survive winter at all (Dijkstra et al., 2007). The early growth phase, from May to July, is initiated by smaller colonies developing from remnants of colonies that survived the cold water (Valentine et al., 2007a). The seasonal growth cycle is also likely influenced by location. For example, the Didemnum sp. growth cycle for colonies in Sandwich tide pool (temperature range from -1 °C to 24 °C, with daily fluctuations), probably does not occur in deep offshore subtidal habitats in Georges Bank (annual temperature range from 4 °C to 15°C, and daily fluctuations are minimal) (Valentine et al., 2007a).  Larval release and recruitment typically occur between 14 to 20°C and slow or cease below 9 to 11°C as summer ends (Griffith et al., 2009; Mckenzie et al., 2017). In New Zealand, recruitment occurs from November to July, where the highest average temperatures were recorded in February (18 to 22°C) and the lowest average temperatures were recorded in July (9 to 10°C) (Fletcher et al., 2013a). In this New Zealand study, higher water temperatures were associated with a higher level of recruitment (Fletcher et al., 2013a).

Didemnum vexillum requires suitable hard substrata for successful settlement and the establishment of colonies. It can grow quickly and establish large colonies of dense encrusting mats on a variety of hard substrata (Valentine et al., 2007a; Griffith et al., 2009; Lambert, 2009; Groner et al., 2011; Cinar & Ozgul, 2023). Gittenberger (2007) stated that invasive Didemnum sp. was a threat to native ecosystems because of its ability to overgrow virtually all hard substrata present. Suitable hard substrata can include rocky substrata such as bedrock gravel, pebble, cobble, or boulders or artificial substrata such as a variety of maritime structures such as pontoons, docks, wood and metal pilings, chains, ropes and moorings, plastic and ship hulls and at aquaculture facilities (Valentine et al., 2007 a&b; Bullard et al., 2007; Griffith et al., 2009; Lambert, 2009; Tagliapietra et al., 2012; Tillin et al., 2020). Didemnum vexillum has been reported colonizing these types of hard substrata in the USA, Canada, northern Kent, and the Solent (Bullard et al., 2007; Valentine et al., 2007a; Valentine et al., 2007b; Hitchin, 2012; Vercaemer et al., 2015; Tillin et al., 2020).

Didemnum vexillum has the ability to rapidly overgrow and displace on other sessile organisms such as other colonial ascidians (Ciona intestinalis, Styela clava, Ascidiella aspera, Botrylloides violaceus, Botryllus schlosseri, Diplosoma listerianium and Aplidium spp.), bryozoan, hydroids, sponges (Clione celata and Halichrondria sp.), anemone (Diadumene cincta), calcareous tube worms, eelgrass (Zostera marina), kelp (Laminaria spp. and Agarum sp.), green algae (Codium fragile subsp. fragile), red algae (Plocamium, Chondrus crispus and bush weed Agardhiella subulata), brown algae (Ascophyllum nodosum, Sargassum, Halidrys, Fucus evanescens and Fucus serratus), calcareous algae (Corallina officinalis), mussels (Mytilus galloprovincialis, Perna canaliculus  and Mytilus edulis), barnacles, oysters (Magallana gigas, Ostrea edulis and Crassostrea virginica), sea scallops (Placopecten magellanicus), or dead shells (Dijkstra et al., 2007; Gittenberger, 2007; Valentine et al., 2007a; Valentine et al., 2007b; Griffith et al., 2009; Carman & Grunden, 2010; Dijkstra & Nolan, 2011; Groner et al., 2011; Hitchin, 2012; Tagliapietra et al., 2012; Minchin & Nunn, 2013; Gittenberger et al., 2015; Long & Groholz, 2015; Vercaemer et al., 2015).

In contrast Didemnum vexillum’s preference for sheltered conditions, established colonies observed in Georges Bank and Long Island Sound were exposed to moderately strong tidal currents (1 to 2 knots; ca 0.5 to 1 m/s recorded at both sites) that may mobilise sediment (Valentine et al., 2007b; Mercer et al., 2009; Tillin et al., 2020). However, Valentine et al. (2007b) describe the substratum as immobile, presumably consolidated gravel, cobbles and pebbles.

Kleeman (2009), stated that the presence of a consistent mild wave action or ‘swash zone’ appears to favour Didemnum sp. establishment in the intertidal. Although some evidence suggests that waves and currents can facilitate the fragmentation and spread of Didemnum vexillum (Mckenzie et al., 2017), the tidal current velocities at some sites where Didemnum vexillum has been reported (for example, New England, where current velocities reach up to around 3 m/s) is lower than the current velocity required for the dislodgement of Didemnum vexillum fragments (around 7.6 m/s) (Reinhardt et al., 2012). This suggests that not all tidal currents are likely to dislodge Didemnum vexillum fragments. When on boat hulls the species can experience higher current velocities which is enough to cause dislodgement (Reinhardt et al., 2012).  

The Sandwich tide pools (USA) were subject to air exposure at low tide, and daily changes in water depth and temperatures (Valentine et al., 2007a). Didemnum vexillum colonies survived exposure to air at low tides for a short time (not exceeding two hours) during rapid colony growth in the summer months July to September (Valentine et al., 2007a). However, parts of the large established colonies, which were artificially exposed to air for two to three hours in October, were observed desiccated or predated on by grazing periwinkles 30 days later, in the winter month of November (Valentine et al., 2007a). They suggested that the invasive tunicates’ ability to tolerate exposure to air varies with the seasonal growth cycle. Didemnum vexillum also tolerated emersion in Kent, as colonies on the mid-shore at Reculver flourish and survive in air exposure for up to three hours per cycle during springs (Hitchin, 2012). Hitchin (2012) suggested the porous nature of the sandstone boulders the species colonized retained water. The Kent shore was sheltered but held water due to its shallow slope and flats, which may allow Didemnum sp. to survive in the low to mid-shore. There is evidence that Didemnum vexillum died when exposed to air for more than 6 hours (Laing et al., 2010).

Didemnum vexillum can overgrow bivalve species, such as oysters, scallops, and mussels, as the hard shells can provide suitable hard substrata for settlement. It has been described as a ‘shellfish pest’ by the aquaculture industry because it is likely to completely encapsulate bivalves and smother them resulting in death or partially encapsulate and partially smother them resulting in reduced bivalve growth (Auker, 2010; Bullard et al., 2007; Coutts & Forrest, 2007, Valentine et al., 2007a; Carman et al., 2009; Kleeman, 2009; Fletcher et al., 2013b; Tillin et al., 2020;). Didemnum vexillum has been recorded overgrowing mussels in Strangford Lough, Northern Ireland (Minchin & Nunn, 2013) and recorded forming large mats over Blue Mussel beds in the Gulf of Maine, completely covering individuals (Auker et al., 2014). Didemnum vexillum fouling on aquaculture equipment and bivalve species causes great economic impacts, as Didemnum vexillum removal methods are expensive, labour-intensive, and not always effective (Coutts & Forrest, 2007; Carman et al., 2009; Kleeman, 2009; Fletcher et al., 2013b; Tillin et al., 2020; Holt, 2024). The fouling on aquaculture nets and bags can restrict water flow and food availability for shellfish and smothering on mussel farms may result in crop losses (Coutts & Forrest, 2007; Carver et al., 2003 cited by Carman et al., 2009; Fletcher et al., 2013b; Holt, 2024). Effects on mussels are likely to become more prominent as Didemnum vexillum becomes more abundant (Auker, 2010).

The epibiotic relationship between Didemnum vexillum and Mytilus edulis negatively impacts mussel growth (Auker, 2010). Clean control mussels with no Didemnum vexillum overgrowth had thicker shells, a significantly thicker lip, and a greater tissue index, compared to mussels overgrown by Didemnum vexillum (Auker, 2010). The clean mussels’ average length ranged from 3.2 cm to 5.37 cm and had significantly greater shell lengths than overgrown mussels, which had an average length from 3.4 cm to 4.86 cm (Auker, 2010). Mortality of both control and overgrown mussels was relatively low over the one-year study period, but higher mortality was seen in overgrown mussels (6.7% died) compared to the clean control mussels (1.1% died) (Auker, 2010). Food is an important factor contributing to the decrease in mussel growth (Auker, 2010). Auker (2010) also found that Didemnum vexillum affected reproduction and recruitment of Mytilus edulis as the invasive species grew over gamete release point (siphons) or inhibited settlement of recruits, but this varied seasonally.

In contrast, the overgrowth of mussels by Didemnum vexillum reduced the predation risk on mussels (Auker, 2010; Auker et al., 2014, Lyu et al., 2020). The Didemnum vexillum mats act as refuges for blue mussels (Lyu et al., 2020). Evidence has suggested that the relationship between Didemnum vexillum and Mytilus edulis reduces the predation by the green crab as Didemnum vexillum deters predator attacks (Auker et al., 2014). It was suggested that the negative impacts of Didemnum vexillum overgrowth on mussel growth, resulting in smaller-sized blue mussels, may protect smaller blue mussels from predation as these are preferred over larger blue mussels by predators (Auker et al., 2014). In Auker’s (2010) study, Carcinus maenas consumed fewer mussels that were overgrown by Didemnum vexillum. The toxic chemical defences of Didemnum vexillum and the release of secondary metabolites and sulfuric acid may deter crab predators (Lyu et al., 2020). The protection from predators provided by Didemnum vexillum may vary seasonally due to evidence suggesting the invasive ascidians deteriorate during the winter months, potentially reducing predation protection for mussels during this time (Auker et al., 2014).

However, Fletcher et al. (2013b) reported that smaller-sized Perna canaliculus mussels (20-40 mm) were significantly affected by fouling of Didemnum vexillum on cultured mussel ropes. The cultured ropes included ambient fouling (ropes left to be naturally colonized by Didemnum vexillum and other species), enhanced fouling (ambient fouling with ropes that were artificially inoculated with Didemnum vexillum) and a control (small levels of fouling maintained by the removal of Didemnum vexillum). The average mussel density and average mussel weight of smaller mussels were higher in the control than in the treatments fouled by Didemnum vexillum. After 15 months, the smaller mussels were significantly smaller than the medium (40-60 mm) and large (60-70 mm)-sized mussels, which remained a similar size by the end of the experiment. They estimated there was a 40% reduction in small-sized mussel density per kilogram of Didemnum vexillum, indicating a negative relationship between small-sized mussel density and increasing Didemnum vexillum.

Small-sized mussels had a significant difference in mussel loss than the larger mussels, with greater loss of the smaller mussels seen in the ambient and enhanced fouling treatments. The small mussels were displaced and overgrown by Didemnum vexillum. Displacement was also evident to a lesser extent in the medium mussels but was less of a threat to larger mussels. However, the fouling treatments alone did not have a significant overall effect on mussel loss. It was suggested that high levels of fouling on the ropes may have resulted in small mussel loss as the mussels carry out a process of self-thinning, but high levels of fouling did not appear to affect individual mussel size or condition directly (Fletcher et al., 2013b). Fletcher et al. (2013b) also noted that Didemnum vexillum clogged cages and mesh used to house shellfish (e.g. mussels and oysters), which could reduce shellfish growth rates. Fletcher et al. (2013b) concluded that there were no direct effects of Didemnum vexillum fouling on mussel size and condition, but did indicate negative effects on small-sized mussels. However, in their study, Didemnum vexillum was only one of the fouling species contributing to fouling effects (Fletcher et al., 2013b).

The Pacific oyster, Magallana (syn. Crassostrea) gigas, is native to warm temperate regions from the northwest Pacific to Japan and northeast Asia, including Cape Mariya (Russia) to Hong Kong (China) (Carrasco & Baron, 2010; GBNNSS, 2011, 2012). It is a fast-growing and tolerant species that has become a successful invader in the coastal waters of all continents, aside from Antarctica (Wrange et al., 2010; Carrasco & Baron, 2010; Padilla, 2010). Magallana gigas is recognised as a beneficial and important species in aquaculture worldwide (Padilla, 2010). It was initially introduced for aquaculture in Europe and the UK in the 1960s due to a decline in the Portuguese oyster (Crassostrea angulata) and the European flat oyster (Ostrea edulis) (Spencer et al., 1994; GBNNSS, 2011, 2012; Humphreys et al., 2014 cited in Alves et al., 2021; Hansen et al., 2023).

Since introduction, the species has invaded and established self-sustaining natural populations throughout Europe from the North Sea, Wadden Sea and Scandinavian coastlines to the Atlantic coastlines of Spain and Portugal, as well as the Mediterranean and Adriatic Sea (Wrange et al., 2010; GBNNSS, 2011, 2012; Ezgeta-Balic et al., 2019; Spagnolo et al., 2019; Bergstrom et al., 2021; Hansen et al., 2023). In the UK, the species predominantly occurs around the southern and western coastlines (OBIS, 2024; NBN, 2024). Shipping activity has also been associated with the introduction of Magallana gigas in the northeastern Adriatic Sea, where it was not introduced for aquaculture (Ezgeta-Balic et al., 2019). It was also suggested that some Magallana gigas populations were established in southwest England from France possibly via fouling on ships (GBNNSS, 2011, 2012; Padilla, 2010; Ezgeta-Balic et al., 2019).

Magallana gigas has a high fecundity, a long-lived pelagic larval phase (2 to 4 weeks) and can produce up to 200 million eggs during spawning (Herbert et al., 2012, 2016; Alves et al., 2021; Wood et al., 2021; Hansen et al., 2023). Hence, as a broadcast spawner, it has a high dispersal potential of more than 1000 km (Padilla, 2010; Wood et al., 2021). Larval mortality can be as large as 99%, as larvae are sensitive to environmental conditions (Alves et al., 2021). But adults are long-lived so that populations can survive with infrequent recruitment (Padilla, 2010). Larval dispersal and mass spawning events have facilitated the settlement and establishment of Pacific oysters, as seen in the Oosterschelde estuary, Netherlands (Hansen et al., 2023). It has been suggested that the spread of the Pacific oyster in Scandinavia is due to northward larval drift on tidal and wind-driven currents (Hansen et al., 2023). Wood et al. (2021) suggested that larval dispersal of the Pacific oyster from populations within and outside the UK was possible via unaided (passive) transport by currents, but that aquaculture and offshore structures (e.g. windfarms) increased the risk of the invasive species spreading and the geographical extent of spread.

Magallana gigas is an ecosystem engineer and can dramatically change habitat structure when it invades. Once successfully settled, groups of Pacific oysters may form dense aggregations, potentially forming a reef, which in some regions can reach densities of 700 individuals/m2 (Herbert et al., 2012, 2016). Once, the density of live or dead Pacific oysters reaches or exceeds 200 ind./m2, little of the underlying substratum remains visible (Herbert et al., 2016). These reefs can stabilize the sediment surface locally (Troost, 2010). When such reefs are formed, or particularly when the species colonizes soft sediments such as mud or sand, it can change and affect local communities, by creating hard substrata for mobile species, which might not otherwise be present before the invasion (Padilla, 2010). However, Hansen et al. (2023) suggested that no immediate ecosystem risk is observed where the Pacific oyster occurs sporadically.

Magallana gigas also colonizes littoral intertidal biogenic reefs formed by the blue mussel Mytilus edulis or honeycomb worm Sabellaria alveolata (GBNNSS, 2011, 2012; Kochmann, 2012; Kochmann et al., 2013; Herbert et al., 2016; Tillin et al., 2020). Evidence suggests the Pacific oyster can out-compete Mytilus edulis, particularly for food and space, as the faster growth rates of the oyster make it more competitive when food or space is limiting (Nehls et al., 2006; Padilla, 2010; Tillin et al., 2020; Joyce et al., 2021). The invasion of Magallana gigas may alter the structure and function of these intertidal reefs but can create a multi-layered structure of a mixture of oysters and blue mussels that is more resilient and accumulates a higher biodiversity of flora and fauna and supports the densities of other native species such as Littorina littorea (Reise et al., 2017; Andriana et al., 2020; Cornelius & Buschbaum, 2020; Hansen et al., 2023). 

Magallana gigas requires hard substrata for successful settlement and establishment, including littoral rock, bedrock, chalk, bare boulders, cobbles and pebbles and shells (Kochmann, 2012; Kochmann et al., 2013; Mckinstry & Jensen, 2013; Herbert et al., 2016; Tillin et al., 2020) because its larvae require hard substrata for successful settlement and development (Mckinstry & Jensen, 2013; Tillin et al., 2020). Invasive populations of Magallana gigas have been found on wave-exposed rocky shores to wave-sheltered soft sediment environments and have been described as habitat generalists (Troost, 2010; Kochmann, 2012; Kochmann et al., 2013). For example, in Scotland, wild Magallana gigas are mainly located in the lower intertidal on bedrock, bedrock encrusted with barnacles, within bedrock crevices, and large and small boulders (Cook et al., 2014). They are unlikely to occur under boulders as they require access to the water column (Tillin et al., 2020). Patches of Pacific oyster reefs have been recorded on littoral rock in Kent, southern England and on littoral sediments in southern England, the North Sea and the English Channel (Herbert et al., 2012, 2016; Morgan et al., 2021).

On littoral rock in Brittany, the Pacific oyster colonizes all intertidal levels from Mean High Water to Mean Low Water on sheltered (low energy), moderately exposed (moderate energy) and high energy rock shores (Herbert et al., 2012). However, in the northwest Pacific, Magallana gigas is commonly found on sheltered low energy littoral rock and has less than 10% cover on exposed high energy littoral rock shores (Herbert et al., 2012, 2016). Magallana gigas has not been found at extreme low water levels or subtidally beneath rocky habitats, as it has been in soft sediment areas (Herbert et al., 2012).

It has been suggested that recruitment is enhanced and abundances are higher in wave-sheltered conditions (Robinson et al., 2005; Ruesink, 2007 cited in Teschke et al., 2020; Tillin et al., 2020). Teschke et al. (2020) found the abundance of Magallana gigas was significantly higher at wave-protected sites within the artificial harbours of Helgoland, North Sea compared to wave exposed sites outside the harbours. In addition, better growth and higher survival rates were observed at wave-protected sites, whereas mortality rates increased at wave exposed sites, due to the wave exposure causing dislodgement or detachment from the settlement substratum (Teschke et al., 2020; Tillin et al., 2020). Similarly, Bergstrom et al. (2021) noted that the occurrence of high densities of both Ostrea edulis and Magallana gigas decreased with increasing wave exposure.

In the Bay of Brest, Pacific oyster reefs on rock had a greater diversity, species richness and biomass than the surrounding bare rock habitats (Lejart & Hily, 2011). There was an increase in macrograzers, suspension feeders, carnivores, deposit and detritus feeders in the present on oyster reefs on rock compared with the surrounding bare rock (Lejart & Hily, 2011). Their results showed that 15% of species present in the oyster reefs on rock were characteristic of mud habitats (Lejart & Hily, 2011). Lejart & Hily (2011) found the surface available for epibenthic species in the Bay of Brest, increased 4-fold when oysters were present on rock, for every 1 m² of colonized substrata the oyster reef added 3.97 m² of surface area on rock. An increase in available settlement substrata, which is free of epibiota, could be why oyster reefs cause an increase in the macrofaunal abundance. Zwerschke et al. (2018) found at intertidal rocky sites and sites with gravel around the UK, Ireland and northern France, densities of Pacific oysters more than 10 m² had a different macrofaunal assemblage structure than sites with low density or no Magallana gigas. Their results showed a greater abundance of species such as barnacles in mud, rock and gravel sites when Pacific oysters were superabundant (oyster density more than 99 /m²).  However, a decrease in the abundance of kelp, Fucus vesiculosus and periwinkle Littorina sp. was observed on the rocky shore sites colonized by the oysters (Zwerschke et al., 2018). In addition, settlement of Magallana gigas in the barnacle zone of exposed rocky shores in the Strait of Georgia, Canada provided a greater surface area for settlement while neighbouring species at the rocky sites facilitated the survival of the Pacific oyster, by reducing predation and physical stress (Ruesink et al., 2005; Herbert et al., 2012).

Similarly, in rocky habitats, in Argentina, four epifaunal species (crabs Cyrtograpsus angulatus, Chasmagnathus granulatus, isopod Melita palmata and snail Helebia australis) showered higher densities and abundance within Magallana gigas beds than outside these areas (Escapa et al., 2004; Herbert et al., 2012).

The South American mytilid Aulocomya ater was reported recently in the Moray Firth, Scotland in 1994 and again in 1997 (McKay, 1994; Holt et al., 1998; Eno et al., 1997). Aulocomya ater is thought to have a stronger byssal attachment than Mytilus edulis and may replace Mytilus edulis in more exposed areas if it reproduces successfully (Holt et al., 1998). However, there is no evidence of competition at present. 

The Australasian barnacle Austrominius (previously Elminius) modestus was introduced to British waters on ships during the Second World War. However, its overall effect on the dynamics of rocky shores has been small as Austrominius modestus has replaced some individuals of a group of co-occurring barnacles (Raffaelli & Hawkins, 1999). Although present, monitoring indicates it has not outnumbered native barnacles in the Isle of Cumbrae (Gallagher et al., 2015) although it may dominate in estuaries (Gomes-Filho, et al., 2010). 

Sensitivity assessment. The Pacific oyster Magallana gigas can colonize all intertidal levels on littoral rock (Herbert et al., 2012) and result in a change in the community depending on density (Ruesink et al., 2005; Lejart & Hily, 2011; Herbert et al., 2012; Zwerschke et al., 2018). The biotope may be altered or replaced. However, Magallana gigas populations may be limited to low densities in very wave exposed to moderately wave exposed conditions (Teschke et al., 2020). On steep or vertical examples of the biotope, densities of Magallana gigas may also be limited as these conditions are less suitable for colonization, suggesting a resistance of ‘Medium’. However, other flat and shallow-sloped examples of the biotope are more suitable for colonization. Therefore, a precautionary resistance of ‘Low’ is suggested for intertidal rock biotopes.  Resilience is likely to be ‘Very low’ as Magallana gigas would need to be physically removed for recovery to occur. Therefore, sensitivity is assessed as ‘High’ for intertidal rock biotopes.

Didemnum vexillum has not been recorded from sites exposed to wave action, that is 'very wave exposed', 'wave exposed' and 'moderately wave exposed' (sensu MNCR, Hiscock, 1998), especially in the intertidal where wave action is not ameliorated by depth (see Hiscock, 1976). Reinhart et al. (2012) examined the effects of water flow and hydrodynamics on the encrusting and tendril forms of Didemnum vexillum. They reported that a current speed of approx. 7.6 m/s was required to induce fragmentation of tendrils but that natural tidal flow alone was insufficient to cause fragmentation of tendrils. They suggested that rare instances of wave action such as storms that resulted in wave orbital velocities of ca 8 m/s or (more likely) human activity could cause fragmentation of tendrils. Reinhart et al. (2012) noted that the tensile strength of Didemnum vexillum was an order of magnitude higher than Botrylloides sp. and was similar to that of Alyconium digitatum. Alyconium digitatum is reported from sheltered to very wave exposed conditions but in the sublittoral. Reinhart et al. (2012) also suggested that seasonal changes in the condition of Didemnum vexillum reduced the tensile strength of colonies and was associated with the period of greater larval production and implied fragmentation aided dispersal. However, in this very wave exposed biotope, the oscillatory nature of wave mediated water flow (wave orbital velocities) combined with wave pressure in the lacerating zone where breaking wave causes, multidirectional strong water movement (Hiscock, 1976) would probably dislodge, and breakup Didemnum vexillum colonies, prevent them from forming suffocating mats, and restrict the colonies to crevices and overhangs, away from the communities that characterize this biotope. Therefore, resistance is assessed as 'High', resilience as 'High' and sensitivity as 'Not sensitive'. However, Hitchin (2012) suggested that the presence of Didemnum vexillum in Whitstable, Kent was contrary to its then known habitat preferences. Therefore, the assessment is made with 'Low' confidence, until further evidence becomes available.

Introduction of microbial pathogens

Benchmark. The introduction of relevant microbial pathogens or metazoan disease vectors to an area where they are currently not present (e.g. Martelia refringens and Bonamia, Avian influenza virus, viral Haemorrhagic Septicaemia virus). Further detail

Evidence

Mytilus species host a wide variety of disease organisms. parasites and commensals from many animal and plant groups including bacteria, blue green algae, protozoa, boring sponges, boring polychaetes, boring lichen, the intermediary life stages of several trematodes, the copepod Mytilicola intestinalis (red worm disease) and decapods e.g. the pea crab Pinnotheres pisum (Bower, 1992; Bower & McGladdery, 1996). Bower (1992) noted that mortality from parasitic infestation in Mytilus sp. was lower than in other shellfish in which the same parasites or diseases occurred. Mortality may result from the shell boring species such as the polychaete Polydora ciliata or sponge Cliona celata, which weaken the shell increasing the mussels vulnerability to predation. Barnacles are parasitised by a variety of organisms and, in particular, the cryptoniscid isopod Hemioniscus balani , in which heavy infestation can cause castration of the barnacle.  At usual levels of infestation these are not considered to lead to high levels of mortality and these are not considered by the sensitivity assessment. Outbreaks of Bonamia may cause significant mortalities in some shellfish populations but this protozoan has been shown not to infect Mytilus edulis (Culloty et al., 1999). 

Marteilia refringens can infect and have significant impacts on the health of Mytilus edulis. There is some debate as to whether there are two species of Marteilia, one which infects oysters (Marteilia refringens) and another that infects blue mussels (Marteilia maurini) (Le Roux et al., 2001) or whether they are just two strains of the same species (Lopez-Flores et al.,2004; Balseiro et al., 2007).  Both species are present in southern parts of the United Kingdom.  The infection of Marteilia results in Marteiliosis which disrupts the digestive glands of Mytilus edulis especially at times of spore release.  Heavy infection can result in a reduced uptake of food, reduced absorption efficiency, lower carbohydrate levels in the haemolymph and inhibited gonad development particularly after the spring spawning resulting in an overall reduced condition of the individual (Robledo et al., 1995). Recent evidence suggests that Marteilia is transferred to and from Mytilus edulis via the copepod Paracartia grani.  This copepod is not currently prevalent in the UK waters, with only a few records in the English Channel and along the South coast.  However, it is thought to be transferred by ballast water and so localised introductions of this vector may be possible in areas of mussel seed transfer.  The mussel populations here are considered to be naive (i.e. not previously exposed) and therefore could be heavily affected, although the likelihood is slim due to the dependence on the introduction of a vector that is carrying Marteilia and then it being transferred to the mussels.

Berthe et al. (2004) concluded that Mytilus edulis is rarely significantly affected by Marteilia sp.  However, occasions have been recorded of nearly 100% mortality when British spat have been transferred from a ‘disease free area’ to areas in France were Marteilia sp. are present.  This suggests that there is a severe potential risk if naive spat are moved around the UK from northern waters into southern waters where the disease is resident (enzootic) or if increased temperatures allow the spread of Marteilia sp. northwards towards the naive northern populations.  In addition, rising temperatures could allow increased densities of the Marteilia sp. resulting in heavier infections which can lead to mortality.

Sensitivity assessment. This assessment solely consideres the sensitivity of Mytilus edulis. Bower (2010) noted that although Marteilia was a potentially lethal pathogen of mussels, most populations were not adversely affected by marteilioisis but that in some areas mortality can be significant in mariculture (Berthe et al., 2004).  The resultant population would be more sensitive to other pressures, even where the disease only resulted in reduced condition.  The removal of clumps of Mytilus edulis would alter the character of the biotope and therefore, a precautionary resistance of ‘Medium’ to this pressure is suggested (<25% mortality), with a resilience of ‘High’ (recovery within 2 years) resulting in a 'Low' overall score for sensitivity.

Removal of target species

Benchmark. Removal of species targeted by fishery, shellfishery or harvesting at a commercial or recreational scale. Further detail

Evidence

The characterizing species Mytilus edulis is too small and patchy in this biotope to be targeted for commercial harvesting. However, some hand-gathering of this species and the edible periwinkle Littorina littorea may occur. As Littorina littorea are present only in low densities and the biotope is wave exposed, ecological effects such as the proliferation of algae are not predicted to arise from its removal.

Sensitivity assessment. Removal of a large percentage of Mytilus edulis by handgatherers would alter the character of the biotope, so that it was more typical of the biotopes, LR.HLR.MusB.Cht.Cht or LR.HLR.MusB.Sem. Resistance is therefore assessed as ‘Low’ and recovery as ‘Medium’, so that sensitivity is assessed as ‘Medium’. 

Removal of non-target species

Benchmark. Removal of features or incidental non-targeted catch (by-catch) through targeted fishery, shellfishery or harvesting at a commercial or recreational scale. Further detail

Evidence

The characterizing species Mytilus edulis is likely to be too small and patchy in this biotope to be targeted for commercial harvesting. However, some hand-gathering of this species and the edible periwinkle Littorina littorea may occur. As Littorina littorea are present only in low densities and the biotope is wave exposed, ecological effects such as the proliferation of algae are not predicted to arise from its removal.  Removal of the characterizing species, Mytilus edulis and barnacles and the red seaweeds accidentally would alter the character of the biotope. The ecological services such as filtation and primary and secondary production provided by these species would also be lost.

Sensitivity assessment.  Removal of a large percentage of the characterising species hwould alter the character of the biotope, so that it was bare rock. Resistance is therefore assessed as ‘Low’ and recovery as ‘Medium’, so that sensitivity is assessed as ‘Medium’.