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

This biotope occurs intertidally and is, therefore, likely to be relatively tolerant of rapid changes in temperature as experienced during cyclical periods of immersion and emersion. Examples of distribution and thermal tolerances tested in laboratory experiments are provided as evidence to support the sensitivity assessment. In general, populations can acclimate to prevailing conditions which can alter tolerance thresholds and care should, therefore, be used when interpreting reported tolerances.

The key characterizing species Cerastoderma edule is found from Norway to Mauritania (Honkoop et al., 2008) and through the Baltic, the Mediterranean and Black Sea (Longshaw & Malham, 2013). The eastern border of distribution is the Murmansk coast of the Barents sea (Genelt-Yanovskiy et al., 2010). The species is, therefore, likely to be exposed to warmer and colder water and air temperatures than experienced in the UK over its geographic range.

Kristensen (1958) reported that Cerastoderma edule from the Dutch Wadden Sea have an upper temperature tolerance of 31°C for 24 hrs, but that spat (3-6 mm) were more tolerant. All cockles died after 6 min at 36°C. Ansell et al. (1981) reported an upper median lethal temperature of 35°C after 24hrs (29°C after 96 hrs exposure), and Wilson (1981) reported an upper lethal temperature of 42.5°C. These temperatures are likely to exceed the pressure benchmark.

Wilson (1981) noted that Cerastoderma edule had limited ability to acclimate and Smaal et al. (1997) stated that Cerastoderma edule is unable to acclimate to low temperatures. However, Newell & Bayne (1980) stated that Cerastoderma edule was able to acclimate to a temperature change of 10°C and regulate its metabolic rate in response to rising spring temperatures. Temperature tolerance in the above studies was dependent on the environmental temperature, i.e. specimens collected in summer or areas of higher average temperature tolerated higher temperatures than specimens collected in winter and/or at lower average temperatures.

Kingston (1974) reared artificially fertilized Cerastoderma edule (as Cardium edule) in the laboratory in the temperature range of 10-20^oC (fertilization did not occur at 5^oC). Larval growth was ‘poor’ at 10^oC, optimal between 15 and 20^oC and most larvae grew poorly and died before metamorphosing at 30^oC. No larval growth occurred at 35 °C and all larvae held at this temperature were dead within 4 days of the start of the experiment.  Honkoop and Van Der Meer (1998) found that winter temperatures influenced egg production by Cerastoderma edule, individuals kept in warmer waters produced smaller eggs.

Wilson (1993) concluded that Cerastoderma edule was probably tolerant of a long-term temperature rise of 2°C associated with climate change. Warmer temperatures during winter result in increased metabolic rate and hence depletion of energy reserves in a time of low food availability and may contribute to post winter mortality of adult cockles (Wilson & Elkaim, 1991). Therefore, the tolerance of Cerastoderma edule to temperature change will be dependent on season, an acute, short-term temperature rise in summer or decrease in winter may be detrimental.

Rapid increases in temperature during the spawning season may initiate spawning (Ducrotoy et al. 1991). High shore populations are likely to be more vulnerable to extremes of temperatures due to their longer emergence time (see emergence). However, Wilson (1981) showed that Cerastoderma edule had the highest upper lethal temperature of the species he studied, presumably due to acclimation from its close contact with the sediment surface. The upper lethal temperature of 42.8°C is unlikely to occur on mudflats except in extremely hot summers.

Changes in temperature may lead to indirect ecological consequences. Experiments demonstrated that predation on Cerastoderma edule by shore crabs (Carcinus maenas) increases as temperature increases (Sanchez-Salazar et al., 1987a) Experiments were run at 6.0, 9.5, and 15.5 ^oC, representing the annual range of sea surface temperatures within the Menai Strait (north Wales).  (Sanchez-Salazar et al., 1987a). Mild winters that enhance predator survival are likely to result in increased predation of spat the following spring (Bukema & Dekker, 2005).,

Other species associated with the biotope may be more tolerant of increased temperatures than Cerastoderma edule. The geographic range of Macoma balthica suggests that the species is tolerant of a range of temperatures and probably becomes locally adapted. In Europe, the species occurs as far south as the Iberian Peninsula and hence would be expected to tolerate higher temperatures than experienced in Britain and Ireland. Oertzen (1969) recorded that Macoma balthica could tolerate temperatures up to 49°C before thermal numbing of gill cilia occurred presumably resulting in death. Ratcliffe et al. (1981) reported that Macoma balthica from the Humber Estuary, UK, tolerated six hours of exposure to temperatures up to 37.5°C with no mortality. It seems likely therefore that the species could adapt to a chronic change and tolerate a large acute change with no mortality.

Field observations and laboratory experiments showed that Macoma balthica spawns (criterion: 50% spent) in spring when the gradual increase of the mean (monthly averaged) water temperature surpasses 8.3°C. The success of spawning and recruitment is affected by the timing of the spring phytoplankton bloom and avoidance of the main settlement of the predator Crangon crangon on intertidal shores (Philippart et al., 2003). A mismatch in spawning cues due to an acute increase in temperature could result in low recruitment or recruitment failures.

Capitella capitata is a dominant species in mud sediments receiving effluents that are typically 8-12°C warmer than the receiving waters (Bamber & Spencer, 1984) and are considered to be tolerant to this pressure at the benchmark. Eteone longa and Pygospio elegans are summer visitors to the same effluent exposed habitats and these three species are considered tolerant of acute and chronic increases in temperature.

Sensitivity assessment. Typical surface water temperatures around the UK coast vary, seasonally from 4-19°C (Huthnance, 2010). The associated species are considered likely to be tolerant of acute and chronic increases in temperature at the pressure benchmark.  Cerastoderma edule has a wide geographic range and as experiments suggest that individuals can survive sudden increases in temperature. As an intertidal species, with some populations occurring above mid-shore, Cerastoderma edule experiences rapid fluctuations in temperature over the tidal cycle. The lack of evidence for mass mortalities in very hot summers (compared with reports for low winter temperatures suggest that this species is likely to tolerate a chronic increase at the pressure benchmark (2°C for one year). An acute increase in temperature for one month may lead to changes in reproductive success and predation, particularly on spat and juveniles. Adults may, however, survive. Biotope resistance is therefore assessed as ‘High’ and residence is ‘High’ (by default), the biotope is therefore considered to be ‘Not sensitive’.

Temperature decrease (local)

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

Evidence

This biotope occurs intertidally and is, therefore, likely to be relatively tolerant of rapid changes in temperature as experienced during cyclical periods of immersion and emersion. Examples of distribution and thermal tolerances tested in laboratory experiments are provided as evidence to support the sensitivity assessment. In general, populations can acclimate to prevailing conditions which can alter tolerance thresholds and care should, therefore, be used when interpreting reported tolerances.

The key characterizing species Cerastoderma edule is found from Norway to Mauritania (Honkoop et al., 2008) and through the Baltic, Mediterranean and Black Sea (Longshaw & Malham, 2013). The eastern border of distribution is the Murmansk coast of the Barents sea (Genelt-Yanovskiy et al., 2010).  Populations at the Barents sea may experience annual water temperatures from 3-8^oC but are exposed to air temperatures of -30°C. These populations are present between mid to low shore and although acclimated to lower temperatures are present in low densities compared to more central parts of the range (Genelt-Yanovskiy et al., 2010). The low densities may be due to thermal tolerances or restrictions on feeding and growth or other factors.

High mortalities of cockle populations due to severe winters have been reported by many authors (Kristensen, 1958; Hancock & Urquhart, 1964; Beukema, 1979, 1985, 1990; Ducrotoy et al., 1991; Strasser et al., 2001). Kristensen (1957) showed a direct influence of temperatures below about -2°C on cockle survival (cited from Beukema, 1979). Kristensen (1958) reported that the sediment froze to a depth of 10 cm and 15 cm, resulting in death of cockles in areas of the Wadden Sea in the severe winter of 1954. Hancock & Urquhart (1964) report almost 100% mortality of cockles in Llanrhidian Sands, Burry Inlet and high mortalities of cockles in other areas around the UK after the winter of 1962/63.  However, enhanced recruitment of bivalves, including Cerastoderma edule and Macoma balthica has been observed in  European estuaries after colder winters while densities following milder winters are lower (Beukema 1991; Walker & Dare, 1993; Young et al., 1996). The factors indirectly responsible for this pattern may be changes in reproductive success (Honkoop & Van Der Meer, 1998), changes in the spring phytoplankton bloom, predation (Beukema & Dekker, 2005), removal of larvae by off-shore currents and removal of adults (enhancing recruitment via reduced ingestion of larvae (André et al.,1993) and reduced competition between adults and juveniles).

The geographical distribution of Macoma balthica suggests that it is very tolerant of low temperature. The species occurs in the Gulfs of Finland and Bothnia where the sea freezes for several months of the year (Green, 1968). It must, therefore, tolerate much lower temperatures than it experiences in Britain and Ireland. Furthermore, Macoma balthica was apparently unaffected by the severe winter of 1962/3 which decimated populations of many other bivalve species (Crisp, 1964), and De Wilde (1975) noted that Macoma balthica kept at 0°C maintained a high level of feeding activity. It is unlikely, therefore, that UK populations of Macoma balthica would be intolerant of decreases in temperature.

Sensitivity assessment. Typical surface water temperatures around the UK coast vary, seasonally from 4-19°C (Huthnance, 2010). The biotope is considered to tolerate a chronic change at the pressure benchmark (2°C decrease in temperature for a year). An acute reduction in temperature may be tolerated by adults and spat outside of winter (although acclimation to warmer temperatures means that impacts on spawning and growth may occur). An acute reduction in temperature during winter may exceed thermal tolerances, biotope resistance (based on Cerastoderma edule) is therefore assessed as ‘Low’ and resistance is assessed as ‘Medium’. Biotope sensitivity is therefore judged to be ‘Medium’, this precautionary assessment is presented in the table.

Salinity increase (local)

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

Evidence

This biotope is reported to occur in full (30-35 ppt) reduced (18-30 ppt) and variable (18-35 ppt) salinity (JNCC, 2015). A change at the pressure benchmark is considered to represent an increase to >40 ppt (the biotope is considered ‘Not sensitive to an increase in salinity from variable or reduced to full).  Little evidence was found for tolerances of elevated salinity although populations are likely to be acclimated to short-term increased salinities in surface sediment layers as evaporation on hot days, or wind driven desiccation leads to increased salinities.

Boyden & Russell (1972) stated that Cerastoderma edule prefers salinities between 15 and 35 psu. Russell & Peterson (1973) reported lower median salinity limits of 12.5 psu and upper median salinity limits of 38.5 psu. Rygg (1970) noted that Cerastoderma edule did not survive 23 days exposure to <10 psu or at 60 psu, although they did survive at 46 psu. Rygg (1970) also demonstrated that salinity tolerance was temperature dependent (after 3 days, 100% survival at 33 psu and 35-38°C, but 50% mortality occurred at 20 psu and 37°C and 100% mortality at 13 psu and 37°C). Wilson (1984) noted that Cerastoderma edule remained open during 1 hour exposure to salinities between 13.3 and 59.3 psu. It should be noted that the tolerances reported above depend on the duration of the experiment.

Kingston (1974) found that Cerastoderma edule larvae grew optimally at 30 and 35 psu, and grew well at 40 psu but the growth increment declined at 45 psu and larvae did not metamorphose. He noted that Cerastoderma edule larvae survived between 20 -50 psu, but died after 11 days at 55 psu or 10 days at 10 psu.

The associated species Macoma balthica is found in brackish and fully saline waters (although it is more common in brackish waters) (Clay, 1967). McLusky & Allan (1976) conducted salinity survival experiments on Macoma balthica (as Macoma balthica) over a period of 150 days. No deaths were reported in specimens of Macoma balthica maintained at 30.5 psu for the duration of the experiment but Macoma balthica failed to grow at 41 psu.

Sensitivity assessment.  Little evidence was found to assess this pressure at the benchmark. Although species within the biotope are likely to tolerate short-term increases in salinity in sediment surface layers between tidal cycles a longer change is likely to exceed salinity tolerances of adults and larvae. Biotope resistance is assessed as ‘Low’ as the results of Rygg (1970) suggest some adults may survive and acclimate. Biotope resilience (following a return to suitable habitat conditions) is assessed as ‘Medium’ and sensitivity is 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

This biotope is reported to occur in full (30-35 ppt) reduced (18-30 ppt) and variable (18-35 ppt) salinity (JNCC, 2015). As the characterizing species are found in biotopes in both full and variable salinity habitats, the biotope is considered ‘Not sensitive’ to a decrease in salinity from full to reduced or variable. The pressure benchmark is assessed as a change to ‘Low’ salinity (<18 ppt). Cerastoderma edule and associated species within this biotope are exposed to periods of potential hypo-saline conditions resulting from heavy rainfall and freshwater runoff. The available studies indicate that Cerastoderma edule larvae and adults show a wide tolerance range of salinity for both adults and larvae, in accordance with the intertidal distribution.  Kristensen (1958), however, reported the death of young spat (1-2 mm) in the Dutch Wadden Sea due to heavy rain, whereas the adults were able to dig deeper into the sediment, reducing exposure.

Boyden & Russell (1972) stated that Cerastoderma edule prefers salinities between 15 and 35 psu. Russell & Peterson (1973) reported lower median salinity limits of 12.5 psu and upper median salinity limits of 38.5 psu. Rygg (1970) noted that Cerastoderma edule did not survive 23 days exposure to <10 psu. Rygg (1970) also demonstrated that salinity tolerance was temperature dependant (after 3 days, 100% survival at 33 psu and 35-38°C, but 50% mortality occurred at 20 psu and 37°C and 100% mortality at 13 psu and 37°C). Wilson (1984) noted that Cerastoderma edule remained open during 1 hour exposure to salinities between 13.3 and 59.3 psu. It should be noted that the tolerances reported above depend on the duration of the experiment.

Russell (1969) found that the optimum salinity for the survival of an adult cockle varies with the mean environmental salinity and suggested that the different salinity tolerance, demonstrated for various populations of Cerastodema  edule are not inherent interspecific differences, but a result of localized environmental acclimation. It is possible that larvae settling in regions of low salinity could have developed elsewhere, under more favourable conditions, and have become gradually acclimatized to the low salinity conditions; alternatively, the larvae produced by parents from a low salinity environment might be adapted to lower salinities than those produced by populations from higher salinity (Russell, 1969).

McLusky & Allan (1976) conducted salinity survival experiments with Macoma balthica (as Macoma balthica) over a period of 150 days. Survival times declined with decreased salinity. At 12 psu, specimens survived 78 days, whilst specimens at 8.5 psu survived 40 days. Some specimens of Macoma balthica survived 2.5 days at 0.8 psu, which was apparently due to the animals ability to clamp its valves shut in adverse conditions. McLusky & Allan (1976) also reported that Macoma balthica failed to grow (increase shell length) at 15 psu. Macoma balthica is found in brackish and fully saline waters (Clay, 1967) so may tolerate a state of flux. Its distribution in combination with the experimental evidence of McLusky & Allan (1976) suggests that Macoma balthica  is likely to be very tolerant to a decreased salinity over a short period. A decline in salinity in the long-term may have implications for the species viability in terms of growth, and the distribution of the species may alter as specimens at the extremes retreat to more favourable conditions.

Sensitivity assessment.  The available evidence suggests that adult Cerastoderma edule may survive a reduction in salinity to just below 18 ppt and populations may become locally acclimated to reduced salinities. As a reduction may lead to some mortalities and a reduction in growth and reproductive success of the key characterizing Cerastoderma edule, biotope resistance is assessed as ‘Medium’, recovery (following a return to usual habitat conditions) is assessed as ‘High’ and sensitivity is therefore assessed as ‘Low’.

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

Cockles are dependent on water flow to deliver suspended food particles. The hydrodynamic regime strongly influences the sediment structure and removal of biodeposits and faeces, oxygenation, food supply and recruitment. Cerastoderma edule prefers muddy-sand to sandy-mud or fine sand substrates. Increases in water flow above the critical erosion rate would re-suspend fine sediments and would alter the habitat.  Increased sediment coarseness would reduce habitat suitability (as assessed below).Decreasing water flow rate in sheltered habitats may increase siltation and favour muddy substrates that are less suitable for Cerastoderma edule. Boyden and Russell (1972) suggested that lack of tidal flow may exclude Cerastoderma edule possibly due to reduced food availability as suggested by Brock (1979). According to regression models developed by Ysebaert et al. (2002), Cerastoderma edule occurs in environments subject to flow velocities of up to 0.8 m/s, having a maximum predicted probability of occurrence at flow velocities around 0.35 m/s.

Newly settled spat and juveniles (<4.8 mm) are capable of bysso-pelagic dispersal., Water flow rates probably affect the distribution and dispersal of juveniles. Increasing water flow may remove adult cockles from the sediment surface and carry them to unfavourable substratum or deep water, where they may be lost from the population. Coffen-Smout and Rees (1999) reported that exposed cockles on the sediment surface could be distributed up to 0.45 m on neap tides or between 94 m and 164 m on spring tides.  Theoretical estimates suggest that the critical force for displacing exposed cockles is 0.3 m/s (Coffen-Smout & Rees, 1999).

Experimental studies of water velocity and clearance rate in Cerastoderma edule have produced a range of results which may be due to genetic or phenotypic differences in test populations (Widdows & Navarro, 2007). Wildish & Miyares (1990) recorded a reduction in flume experiments found that feeding efficiency was greatest at 0.15 m/s and gradually declined to 0.45 m/s, there was no significant difference in feeding rate between current velocities of  0.05 and 0.35 m/s(Widdows & Navarro, 2007). At 0.45 m/s, sand grains (1-3 mm) began to roll along the bed and this may have reduced clearance rate. At 0.7 m/s, feeding appeared to cease due to the movement of sediment as well as cockles (Widdows & Navarro, 2007).

Sensitivity assessment. The associated burrowing species are considered to be ‘Not Sensitive’ to this pressure, as burrowing life habits coupled with deposit or predatory feeding types were considered to be protective. Many of these species are also found on mudflats and hence have little to no sensitivity to this pressure as species-specific habitat suitability would not decrease. The characterizing Cerastoderma edule were considered to have some resistance to this pressure as they are found within a range of flow speeds and can feed at a range of flow speeds. However decreased flow rates (at the pressure benchmark) in sheltered habitats may reduce food supply and enhance sediment deposition favouring deposit feeders. At the pressure benchmark some biotopes may be affected by an increase or decrease at the pressure benchmark through effects on sediment and delivery of suspended food, biotope resistance is assessed as 'Medium' and resilience is assessed as 'High' as the changes may be outweighed by seasonal events such as storms. Therefore, sensitivity is assessed as 'Low'.

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

Cockle dominated biotopes can range from mean high water springs (Sanchez-Salazar et al., 1987b) to the sublittoral (JNCC, 2015).  Shore height influences a number of factors that affect cockle condition and survival and the size and age structure of populations can vary significantly with shore height (Sanchez-Salazar et al., 1987b), hence, this biotope is likely to be sensitive to changes in emergence (both increase and decrease). 

At lower shore levels predation by shore crabs and fish may structure populations by removing smaller individuals and may set the lower distribution limit while at higher shore levels predation by oystercatchers targets larger size classes (Sanchez-Salazar et al., 1987b). Shore height will also influence emergence times, higher shore populations are exposed to air temperatures for longer that may be warmer and colder than seawater creating thermal shocks, higher shore individuals will also have less time to feed, resulting in reduced growth (Jensen, 1992) body condition which may increase susceptibility to parasites and other factors (Wegeberg & Jensen, 2003). Dense populations lower on the shore may also deplete the available suspended food, reducing the supply to higher shore populations (Peterson & Black, 1987, 1991; Kamermans, 1993).

DeMontadouin and Bachelet (1996) manipulated low and high population densities (160-2000 adults/m² and tidal elevation (low and mid-water levels of Cerastoderma edule at Arcachom bay, SW France to test the influence of adult densities and emersion time on growth, settlement and survival. Growth rates were affected by tidal height with higher growth rates at low water levels.

Sensitivity assessment. A change in emersion is likely to alter the habitat suitability for Cerastoderma edule and associated species, resulting in changes in assemblage structure, biotope resistance is therefore assessed as ‘Low’ and resilience is assessed as ’Medium’ following a return to previous habitat condition. Biotope 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

This biotope is recorded from locations that are judged to range from extremely sheltered to moderately exposed (JNCC, 2015).  As the biotope and characterizing and associated species are found across a range of wave exposures, populations occurring within the middle of the range are considered to have 'High' resistance to a change in significant wave height at the pressure benchmark. Resilience is assessed as ‘High’, by default, and the biotope is considered ‘Not sensitive’ Changes in wave exposure greater than the pressure benchmark are likely to have marked effects on the sediment dynamics of the shore. Increased exposure could result in increased grain size or erosion of the sediment while decreased exposure will lead to increased siltation and reduced grain size (muddy sediment). In both cases, the sediment may become unsuitable for Cerastoderma edule populations resulting in a reduction of the extent or abundance of the population (see physical change pressures). Increased wave action during storms may also remove adult cockles from the sediment surface which may be subsequently lost from the population. These changes are not assessed in this section as they are considered to be the result of changes in wave action that exceed the pressure benchmark.

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

The results of the Rapid Evidence Assessment on the effects of 'Transitional metal or organometal' contaminants on selected polychaete and mollusc species are summarized below. The full 'evidence reviews' should be consulted for details of the studies examined and their results. A sensitivity assessment is provided for each type or source of 'Transitional metal or organometal' contaminant examined, together with an overall pressure assessment. 

Transitional metals. ‘Severe’ or ‘Significant’ mortality was reported in 88% of the results from studies of the effects of ‘Transitional metals’ exposure on Cerastoderma edule depending on the exposure concentration or duration of all the ‘metals’ studied, with the exception of manganese (Mn). Bryan (1984) suggested that many polychaetes were resistant to heavy metals and evidence from the work of Bryan & Gibbs (1983) in the metal polluted Fal estuary supports this view. Bivalves, on the other hand, including Cerastoderma edule displayed a much lower tolerance and were found to be the most obvious absentees from the polluted Restronguet Creek area of the Fal (Bryan & Gibbs, 1983). Adult Cerastoderma edule were found to be more tolerant to metal toxicity than the juvenile or larval stages which appear unable to withstand the high concentrations of copper and zinc. Studies of Cerastoderma edule transplanted from polluted and uncontaminated sites resulted in 10-15% mortality within 63 days but 100% within 4 months at the Restronguet Creek (Bryan & Gibbs, 1983). Bryan & Gibbs (1983) stated that Cerastoderma edule takes up heavy metals mainly from solution rather than from sediment and that it was excluded from Restronguet Creek by the high levels of Cu and Zn. Bryan (1984) stated that Hg was the most toxic metal to bivalves. In addition, Cu and Zn are believed to inhibit the settlement of juvenile Cerastoderma edule, leading to patchy distributions (Langston et al., 2003). Studies of Cerastoderma edule populations from polluted and un-contaminated sites in Southampton Water showed that tissue heavy metal concentrations were lower in summer than winter/spring, tissue heavy metal concentrations decreased with the size of the cockle, and cockles in sediments contaminated with metals and hydrocarbons had lower life expectancies, growth rates and body condition index (Savari et al., 1991a,b).

Barite (in the form of drilling mud barite) was shown to cause 100% mortality of Cerastoderma edule within 12 days at a depth of 2- and 3-mm dosage but the cause may have been due to physical damage of their gill filaments rather than chemical toxicity (Barlow & Kingston, 2001). Ladhar-Chaabouni et al. (2009) was the only article to examine Cerastoderma glaucum but reported that cadmium (Cd) exposure resulted in 100% mortality 18 days after exposure to 100 µg/l Cd.  Overall, the evidence suggests that the worst-case resistance of Cerastoderma spp. to ‘transitional metals’ exposure is ‘None’. Therefore, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’.

‘Severe’ or ‘significant’ mortality was reported in 52% of the results from studies of the effects of ‘Transitional metals and organometal’ exposure on Macoma spp. depending on the exposure concentration or duration. Copper and cadmium were reported to result in ‘severe’ mortality, while arsenic, chromium, mercury, silver, zinc, and nickel were reported to result in ‘significant’ mortality, depending on concentration, duration, and environmental conditions. The remaining metals were reported to result in no mortality or sublethal effects (see evidence review). As above, barite (in the form of drilling mud barite) was shown to cause 100% mortality of Macoma balthica within 12 days at a depth of 2- and 3-mm dosage but the cause may have been due to physical damage of their gill filaments rather than chemical toxicity (Barlow & Kingston, 2001). Overall, the evidence suggests that the worst-case resistance of Macoma spp. to ‘transitional metals’ exposure is ‘None’. Therefore, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’.

Rygg (1985) classified Scoloplos armiger, Capitella capitata and Eteone longa as highly tolerant species, common at the most copper polluted stations (Cu >200 mg/Kg) in Norwegian fjords. Bryan & Gibbs (1983) found that Pygospio elegans appear to have adapted to the very high concentrations of copper and zinc in Restronguet Creek in the highly contaminated Fal estuary and the larvae are subjected to widely fluctuating conditions of salinity and relatively high metal concentrations.

A 2-year microcosm experiment was undertaken to investigate the impact of Cu on the benthic fauna of the lower Tyne Estuary (UK) by Hall and Frid (1995). During a 1-year simulated contamination period, 1 mg l−1 Cu was supplied at 2-weekly 30% water changes, at the end of which the sediment concentrations of Cu in contaminated microcosms reached 411 μg g−1. Toxicity effects reduced populations of the four dominant taxa, including Capitella capitata. When Cu dosage was ceased and clean water was supplied, sediment Cu concentrations fell by 50% in less than 4 days, but faunal recovery took up to 1 year, with the pattern varying between taxa. Since the Cu leach rate was so rapid it is concluded that after remediation, contaminated sediments show rapid improvements in chemical concentrations, but faunal recovery may be delayed with experiments in microcosms showing faunal recovery taking up to a year.

In a review of chemical use on salmon aquaculture, Burridge et al. (2010) described how despite the binding of copper in sediments, it can be toxic (copper is used as an antifoulant and may also be a constituent of the food fed to farmed salmon). Sediments under salmon cages in the Bay of Fundy and at various distances away from the cages were evaluated for toxicity and in addition to elevated levels of copper (above the threshold effects level), the sediments also had elevated zinc, other metals, ammonia nitrogen, sulphide, total organic carbon, and other organic compounds. Sediments enriched in copper, zinc and silver caused decreased reproduction in the clam Macoma balthica, due to failed gamete production. Reproductive recovery occurred when contamination decreased (Hornberger et al., 2000). It was noted that studies from field sites have numerous metals rather than just copper alone, and it is difficult to attribute toxicity to any particular metal.

Organometals. Beaumont et al. (1989) examined the effects of tributyltin (TBT) exposure in Cerastoderma edule and Macoma balthica. In their flow-through mesocosm studies, all Cerastoderma edule died within two weeks at high concentrations of TBT (1-3 µg/l) and progressive mortality was observed in the low TBT treatments (0.06-0.17 µg/l) over time with 80% mortality after 17 weeks. However, unlike Cerastoderma edule, no mortality was reported and some juvenile Macoma recruited to the low (0.06-0.17 µg/l) TBT treatment mesocosm. Therefore, the worst-case resistance of Cerastoderma spp. to TBT exposure is assessed as ‘None’, resilience as ‘Medium’ and sensitivity as ‘Medium’, especially long-term exposure, while Macoma balthica may be considered 'Not sensitive' at the concentrations studied. However, confidence in the assessment is ‘Low’ due to the limited number of studies reviewed.

Overall sensitivity assessment for this pressure. The worst-case resistance of the dominant characteristic species Cerastoderma edule is 'None' based on the evidence of the effects of 'transitional metals' and 'organometals', depending on the concentration and duration of exposure.  Hence, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’. 

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

The results of the Rapid Evidence Assessment on the effects of 'Hydrocarbons & PAHs' contaminants on selected polychaete and mollusc species are summarized below. The full 'evidence reviews' should be consulted for details of the studies examined and their results. A sensitivity assessment is provided for each type or source of 'Hydrocarbons & PAHs' contaminant examined, together with an overall pressure assessment. 

Oil spills. High mortalities of the cockle Cerastoderma edule were reported following the Sea Empress oil spill in Milford Haven, Wales, and large numbers of moribund and dead marine animals, including Cerastoderma edule, were washed ashore after the Sea Empress oil spill. However, no commercial stocks were affected (Rostron, 1998). In Angle Bay, the presence of juveniles lower down the shore shortly after the spill enabled the re-establishment of adult populations on the middle shore within about six months. Additional species recorded at Sandy Haven in the summer following the spill included the polychaetes Pygospio elegans and Capitella capitata: the abundance of Capitella capitata increased dramatically at one site (Rostron, 1998).

Hydrocarbons and PAHs, including dispersants. Studies of the effects of Hydrocarbons or PAHs’, on Cerastoderma edule contributed 98% of the results (worst-case ranked mortalities) on this pressure in the evidence review, of which 27% reported ‘severe’ mortality and 73% reported ‘significant’ mortality. Most (74%) of the results were from studies that examined the effects of dispersants and emulsified oils, which reported ‘severe’ or ‘significant’ mortality in all cases. ‘Severe or ‘significant’ mortality was also reported due to exposure to complex hydrocarbons, phenols, and a PAH (phenanthrene) in Cerastoderma edule. ‘Significant mortality was also reported in Cerastoderam glaucum.  Laboratory studies demonstrated that Cerastoderma edule is sensitive to oil and polycyclic aromatic hydrocarbons (Wootton et al., 2003) and the available evidence indicated that Macoma balthica was also sensitive to acute and chronic exposure. Some of the polychaetes associated with this biotope are either more tolerant of hydrocarbons (Eteone longa) or their populations are able to recover rapidly (Pygospio elegans and Capitella capitata).

McLusky (1982) examined the fauna of the intertidal mudflats at Kinneil in the Forth estuary that received petroleum, chemical and domestic effluents. Spatfall of Cerastoderma edule occurred in 1976 but the abundance declined steadily between 1976 and 1980. Cerastoderma edule, together with many other species, was excluded from sediment within 1.5 km of effluent discharges. Between 1.5-2.25 km of the discharges, the abundance of fauna, including Cerastoderma edule increased markedly (McLusky, 1982).

Stekoll et al. (1980) exposed the associated species, Macoma balthica, to Prudhoe Bay crude oil in flowing seawater for six months at three concentrations; low 0.03 mg/l, medium 0.3 mg/l and high 3.0 mg/l and concluded that chronic exposure of Macoma balthica to oil-in-seawater concentrations even as low as 0.03 mg/l would in time lead to population decreases. The individuals in this study were not subjected to any of the stresses that normally occur in their natural environment on mudflats such as changes in salinity, temperature, oxygen availability and wave action, therefore, it is possible that exposure of Macoma balthica to oil under field conditions results in higher mortality.

Shaw et al. (1976) also reported mortality of Macoma balthica caused by exposure to crude oil following an experimental application of oil at a concentration of 1.2 µl oil/cm² and 5.0 µl oil/cm² to sediments which equated to oil spills of one ton /20 km² and one ton/100 km². Significant mortalities were observed after only two days following the application of the oil at a concentration of 5.0 µl oil/cm². Some specimens of Macoma balthica survived the application of oil in these experiments but were weakened.

Eteone longa was described by Hiscock et al. (2005) (based on Levell et al., 1989) as a very tolerant taxon to oil pollution and was found in enhanced abundances in the transitional zone along hydrocarbon contamination gradients surrounding oil platforms.

Only one article (Farke & Gunther, 1984) examined the effects of dispersants on Macoma balthica. No mortality was reported and it was unclear what effects the dispersant had on the population based on the data alone. Therefore, the evidence was not adequate to support an assessment of Macoma's sensitivity to dispersants.  

Overall sensitivity assessment. The worst-case resistance of the dominant characteristic species Cerastoderma spp. to ‘Hydrocarbons and PAHs’ is assessed as ‘None’. Hence, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’. Confidence in the assessments is assessed as ‘Medium’ because only the data rather than the original data sources were accessible.  The worst-case resistance of Macoma spp. to petroleum hydrocarbons is assessed as ‘Low’, resilience as ‘High’ and sensitivity as ‘Low’ but with ‘Low’ confidence due to the limited number of studies reviewed.

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

The results of the Rapid Evidence Assessment on the effects of 'Synthetic compound' contaminants on selected polychaete and mollusc species are summarized below. The full 'evidence reviews' should be consulted for details of the studies examined and their results. A sensitivity assessment is provided for each type or source of 'Synthetic compounds' contaminant examined, together with an overall pressure assessment. 

Pesticides/biocides. All three of the studies that examined exposure of Cerastoderma edule to ‘Pesticides/biocides’ reported ‘severe’ or ‘significant’ mortality. Goncalves et al. (2016) reported 96-hour LC50 values of 28.78 mg/l (large specimens) and 27.25 mg/l (small) and 100% mortality at 60 mg/l in Cerastoderma edule exposed to the herbicide Primextra® Gold TZ. Portmann & Wilson (1971) and Portmann (1972) exposed Cerastoderma edule to a range of different ‘Pesticides/biocides’ (see Mollusc Evidence Summary). Overall, the evidence suggested that Cerastoderma edule was sensitive to all the ‘Pesticides/biocides’ tested. Therefore, the worst-case resistance of Cerastoderma edule to ‘Pesticides/biocides’ is assessed as ‘None’. Hence, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’. However, confidence in the assessment is ‘Medium’ due to the limited number of studies reviewed.

Three articles examined the effects of ‘Pesticides/biocides’ on Macoma spp. Armstrong & Millemann (1974) exposed Macoma nasuta to Sevin at 15, 20, 25, and 30 mg/l for 96 hours.  After 96 hours of exposure around 50% of the clams had withdrawn one or both siphons, with estimated 48-hour and 96-hour EC50s of 27.5 and 17 mg/l Sevin, respectively. But no mortality was reported. Boese et al. (1990) reported sublethal effects on the physiology of Macoma spp. exposed to 5.2 – 7.8 µg/l hexachlorobenzene for 3-7 days. Dumbauld et al. (2001) examined the effects of pesticide treatment of oyster sites on benthic infauna.  No significant effects on Macoma spp. abundance were observed 24 hours, 2 weeks, 1 month and 1 year after the application of Carbaryl at 5.6 kg/ha. The average density of Macoma spp. was significantly different from the control plots at 51 days post-exposure to 8.4 kg/ha Carbaryl but there were no significant differences after 2 days or 1 year (Dumbauld et al., 2001). Therefore, the worst-case sensitivity of Macoma spp. to the ‘Pesticides/biocides’ tested is assessed as ‘Not sensitive’ since only sublethal or transient effects were reported. However, confidence in the assessment is ‘Low’ due to the limited number of studies and pesticides tested.

Nephtys spp., Eteone longa, and Streblospio benedicti were examined in only two of the articles reviewed. Only sublethal effects were reported. For example, Dumbauld et al. (2001) observed the effects of the application of the pesticide Carbaryl on the estuarine benthic community in oyster culture sites but did not detect trends or significant differences in the abundance of the polychaetes Streblospio benedicti and Eteone longa. Similarly, Scanes et al. (1993) reported no significant changes in polychaete abundance after an accidental spill of the pesticide Aldrin on an estuarine beach in New South Wales, Australia. 

Pharmaceuticals. Lusher et al. (2017) did not find any significant differences in the condition index, nor any evidence of intersex in Cerastoderma edule exposed to bisphenol-A and 17b-oestradiol. However, 17b-oestradiol exposure (at 0.1 µg/l for 60 days) did result in ‘some’ mortality compared to the control. Therefore, the worst-case resistance of Cerastoderma edule to the human hormone 17b-oestradiol is assessed as ‘Medium’ but with ‘Low’ confidence due to the limited evidence. Hence, resilience is probably ‘High’ and sensitivity is assessed as ‘Low’.

PCBs. Portmann & Wilson (1971) and Portmann (1972) exposed Cerastoderma edule to a range of different ‘PCBs’ (see Mollusc Evidence Summary). Their 48-hour LC50 ranged from 3 to 10 mg/l depending on the PCB. Therefore, the worst-case resistance of Cerastoderma edule to ‘PCBs’ is assessed as ‘Low’. Hence, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’. However, confidence in the assessment is ‘Medium’ due to the limited number of studies reviewed.

Others. Maggi & Cossa (1973), Portmann & Wilson (1971) and Portmann (1972) examined the effects of a number of alcohols and surfactants on Cerastoderma edule adults and larvae. The articles were not accessible, but the data was provided by ECOTOX and included in the ‘Mollusc Evidence Summary’ spreadsheet. Methanol exposure resulted in a 48-hour LC50 of 1,000 mg/l in adult Cerastoderma edule while exposure to 2-Propen-1-ol resulted in a 48-hour LC50 of 100 mg/l in adult and larvae (Portmann & Wilson, 1971; Portmann, 1972). Therefore, the worst-case resistance of Cerastoderma edule to the alcohols tested is assessed as ‘Low’, resilience as ‘Medium’ and sensitivity as ‘Medium’. However, it should be noted that the concentrations used were high and the confidence in the assessment is ‘Low’. Maggi & Cossa (1973), Portmann & Wilson (1971), and Portmann (1972) also derived lethal doses (LD50s) and LC50s for a number of surfactants. Therefore, the worst-case resistance of Cerastoderma edule to the surfactants tested is assessed as ‘Low’, resilience as ‘Medium’ and sensitivity as ‘Medium’. However, the confidence in the assessment is ‘Low’ due to the limited evidence.

Overall sensitivity assessment for this pressure. Cerastoderma edule was reported to be sensitive to all the pesticides/biocides studied (see evidence review) while Macoma spp. was not. Cerastoderma was also shown to be sensitive to a range of PCBs, some alcohols and surfactants and, possibly, the human hormone 17b-oestradiol.  Therefore, the worst-case resistance of the dominant characteristic species Cerastoderma edule to 'synthetic compounds' is assessed as 'None', based on the evidence from pesticide/biocide exposure. Hence, resilience is assessed as 'Medium' and sensitivity as 'Medium'.  However, the confidence in the assessment is 'Low' due to the variation in effects between chemicals, depending on the concentration and duration of exposure, and the limited number of studies reviewed. 

Radionuclide contamination

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

Evidence

No evidence was found

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

The results of the Rapid Evidence Assessment on the effects of 'Other substances' contaminants on selected polychaete and mollusc species are summarized below. The full 'evidence reviews' should be consulted for details of the studies examined and their results. A sensitivity assessment is provided for each type or source of 'Other substance' contaminant examined, together with an overall pressure assessment. 

Inorganic chemicals. Portmann & Wilson (1971) examined the effect of a number of inorganic chemicals (disinfectants) on Cerastoderma edule. The 48-hour LC50s were as follows: 330 to 1,000 mg/l nitric acid; 25 mg/l potassium cyanide; 66,000 mg/l sodium chloride; 330 to 1000 mg/l sodium hydroxide; of >500 mg/l sodium thiocyanate; >500 mg/l chlorine dioxide (ClO2), and 200 to 500 mg/l sulphuric acid. Therefore, the worst-case resistance of Cerastoderma spp. would be assessed as ‘Low’, so resilience is probably ‘Medium’ and sensitivity ‘Medium’. However, confidence is ‘Low’ since the evidence is based on a single study and the concentrations used are high. For example, GESAMP (2019) criteria describe EC/LC50 values of >100 – ≤1000 mg/l as ‘Practically non-toxic’. Caldwell (1975) exposed Macoma balthica to 100, 3,30, 1000, 3,300, and 10,000 µg/l hydrogen sulphide for 96 hours. The longer the clams were exposed to hydrogen sulphide the lower the concentration was required to cause 50% mortality. The LC50 at 24, 48, and 96 hours were 10,000, 8,000 and 6,000 µg/l respectively. Crecelius (1979) examined the effect of bromate on Macoma inquinata and reported 100% mortality after 72 hours at 880 mg/l bromate. Therefore, the worst-case resistance of Macoma spp. to the inorganic chemicals tested is assessed as ‘None’, resilience as ‘Medium’ and sensitivity as ‘Medium’ but with ‘Low confidence due to the limited evidence.

Paint particles. Muller-Karanassos et al. (2021) investigated the effects of environmental concentrations of antifouling paint particles on sediment-dwelling invertebrates. Adult ragworms and cockles were exposed to three types of antifouling paint particles (APP), two biocidal (‘historic’ and ‘modern’) and one biocide-free (‘silicone’). Two laboratory-based 18-day and 5-day exposure experiments were carried out. The APPs ranged in particle size and included varying concentrations of Cu, Sn, Pb, Hg, and Zn. Trial experiments carried out using the maximum environmental APP concentration (18.8 g/l) caused 100% mortality of all ragworms and cockles in the modern treatment within 6 days. In the 18-day exposure, antifouling paint particle concentrations were 4.2 g/l for the historic biocidal treatment; 3.0 g/l for the modern biocidal treatment; and 2.1 g/l for the non-biocidal silicone treatment. The burrowing rate of the ragworms was reduced by 29% in the modern biocidal treatment. However, there were no significant differences between treatments. Ragworms decreased in weight and feeding rates significantly, but significant differences were only seen between the modern biocidal treatment and the control. Modern biocidal antifouling paint particles were used at concentrations ranging from 0 to 30 g/l (ragworms) and 0 to 6 g/l (cockles) to estimate the 5-day LC50 exposure. The 5-day LC50 values were 19.9 g/l for the ragworms and 2.3 g/l for cockles. The 5-day EC50 values were 14.6 g/l for the ragworms and 1.4 g/l for cockles. The evidence Muller-Karanassos et al. (2021) suggests that antifouling paint particles remain toxic in the environment. Therefore, the resistance of Cerastoderma edule to APPs is assessed as ‘None’. Hence, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’ but confidence in the assessment is ‘Low’ due to the lack of evidence.

Mixtures. ‘Mixtures’ include articles that have assessed the impacts of wastewater discharge, pulverized fuel ash, industrial effluent, fish farm effluents and polluted sites on the selected molluscs. Bergayou et al. (2019) observed the changes in an estuarine ecosystem following the cessation of wastewater discharge. Three campaigns were undertaken, two were carried out while the estuary was receiving wastewater discharge in 2001 and 2002, and one campaign was carried out after the cessation of the pollution in 2003. When the ecosystem was receiving wastewater discharge, the intertidal macrobenthic fauna composition was similar, with Hydrobia ulvae as the dominant species, followed by Hediste diversicolor and Scrobicularia plana in decreasing order. After the termination of wastewater discharge, the number of individuals was significantly higher than in the period when the ecosystem received wastewater. In 2003, the dominance of species was Hediste diversicolor, followed by Hydrobia ulvae, Cerastoderma edule, and Scrobicularia plana in decreasing order. However, both before and after the end of wastewater discharge, the Phylum Mollusca was dominant, followed by Annelids and Crustaceans. The species richness was higher in 2003 following the end of the wastewater discharges, with 22 species instead of 14. The total abundance percentage of Cerastoderma edule increased from <4 % in 2001 and 2002 to 23% in 2003.

Bowmer et al. (1994) investigated the effects of Pulverized Fuel Ash (PFA) exposure on the cockle Cerastoderma edule for 3 and 9 months. The impacts on survival, growth, metal accumulation, and histology were investigated using model ecosystem experiments. The cockles were exposed to 100% PFA or 50% PFA. After 230 days, the mortality rate of the 100% PFA treatment was 43%, and the mortality rate of the 50% PFA treatment was 42.5%. The growth of the cockles exposed to PFA treatments was notably reduced compared to the control. Jenner & Bowmer (1990) investigated the effects of Pulverized Fuel Ash (PFA) exposure on Arenicola marina, Cerastoderma edule, and Macoma balthica. The impacts on survival and metal accumulation were investigated through 90-day mesocosms experiments. The test organisms were exposed to 100% PFA, 50% PFA or dosed daily with 500 ml PFA. After 90 days, the mortality rate of Cerastoderma edule at 100% PFA treatment was 43.3%, the mortality at 50% PFA was 31.7% and the mortality in the dosed treatment was 70.6%. The control mortality was 26%. In Macoma balthica, mortality could not be followed in three of the treatment tanks because a substantial wild population of Macoma balthica still survived in all mesocosms. However, there was 20% mortality reported in the 100% PFA treatment. 

Overall, wastewater discharge was shown to reduce the abundance of Cerastoderma edule and Macoma cumana in the affected area (Bergayou et al., 2019). Exposure to pulverised fuel ash was reported to result in ‘Severe’ mortality in Cerastoderma edule (Jenner & Bowmer, 1990; Bowmer et al., 1994), while pollution in Southampton Water resulted in reduced scope for growth (Savari et al., 1991). However, the exact nature of the contaminants in each mixture is unclear.  Therefore, the worst-case resistance of Cerastoderma edule to pulverised fuel ash exposure is assessed as ‘None’, resilience as ‘Medium’ and sensitivity as ‘Medium’ but with ‘Low’ confidence. However, its resistance to wastewater discharge may be ‘Medium’ and its sensitivity ‘Low’ depending on the nature of the contaminants involved but confidence is ‘Low’ due to the lack of evidence. The worst-case resistance of Macoma balthica to pulverised fuel ash exposure is assessed as ‘Medium’, resilience as ‘High’, and sensitivity as ‘Low’ but with ‘Low’ confidence. However, its resistance to wastewater discharge may be ‘Medium’ and its sensitivity ‘Low’ depending on the nature of the contaminants involved but confidence is ‘Low’ due to the lack of evidence. 

Overall sensitivity assessment for 'Other substances'. The sensitivity of the dominant characteristic species Cerastoderma edule to 'other substances' varies with the 'substance' studied, its concentration and duration of exposure.  The worst-case resistance of Cerastoderma spp. to 'other substances' is assessed as 'None' based on the effects of inorganic disinfectants, and anti-fouling paint particles. Hence, resilience is assessed as 'Medium' and sensitivity as 'Medium'. However, confidence in the assessment is 'Low' due to the variation in the effect of different chemicals and the limited number of studies reviewed. 

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

Muddy sands may have relatively low oxygen concentrations, lower than coarse sands but higher than muds. The effects of changes in dissolved oxygen concentration on the marine environment can be sub-divided into direct effects (those organisms directly affected by changes in dissolved oxygen concentration) and secondary effects (those arising in the ecosystem as a result of the changes in the organisms directly affected). The direct effects of changes in dissolved oxygen (DO) concentrations are primarily related to reduced DO levels and include lethal and sub-lethal responses in marine organisms, the release of nutrients, and the development of hypoxic and anoxic conditions. Anaerobic conditions in the sediments increases microbial activity and reduces the redox potential of the sediments (Fenchel & Reidl, 1970). Ultimately this increases the production of toxic chemicals such as hydrogen sulphide and methane. The changed status to anaerobiosis will limit the sediment macroinfauna to species which can form burrows or have other mechanisms to obtain oxygen from overlying water. Anoxic conditions may alter community structure and reduce diversity and abundance and interfere with bird feeding (Simpson, 1997, cited in Elliott et al., 1998).

A number of animals have behavioural strategies to survive periodic events of reduced dissolved oxygen. These include avoidance by mobile species such as crustaceans, shell closure and reduced metabolic rate in bivalve molluscs and either decreased burrowing depth or emergence from burrows for sediment dwelling crustaceans, molluscs and annelids. The sensitivity to reduced oxygen and recovery from episodes of hypoxia and anoxia varies between the characterizing and associated species of this biotope. The available evidence suggests that Cerastoderma edule is more sensitive to this pressure than Macoma balthica and the polychaete species.

Rosenberg et al. (1991) reported 100% mortality of Cerastoderma edule exposed to 0.5-1.0ml/l oxygen for 43 days and 98% mortality after 32 days. Cerastoderma edule migrated to the surface of the sediment in response to decreased oxygen concentrations. Theede et al. (1969) reported 50% mortality after 4.25 days at 1.5 mg/l oxygen. Theede et al. (1969) also noted that Cerastoderma edule only survived 4 days exposure to 0.0-6.1 cm³/l of hydrogen sulphide, which is associated with anoxic conditions. This suggests that Cerastoderma edule could survive short periods of anoxia but it is likely that continued exposure to 2 mg/l oxygen for a week would be lethal.

Fifty percent (LT50) of cockles in anoxic seawater died after 3.5 days (Babarro & de Zwaan, 2001) The anoxic survival time of Cerastoderma edule from two different ecosystems and differing anoxia tolerances was studied in static (closed) and flow-through systems. The antibiotics chloramphenicol, penicillin and polymyxin were added, and molybdate ( a specific inhibitor of the process of sulfate reduction). Median mortality times were 2.7 and 2.9 days for Cerastoderma for static and flow-through incubations, respectively. The addition of chloramphenicol increased strongly survival time in both systems with corresponding values of 6.4 and 6.5 days for Cerastoderma. Overall the results indicate that proliferation of anaerobic pathogenic bacteria, associated with the bivalves, is a main cause of death besides the lack of oxygen. Bacterial damage is probably caused by injury of the tissues of the clams and not by the release of noxious compounds to the medium (de Zwaan et al. 2002).

Macoma balthica appears to be relatively tolerant of deoxygenation. Brafield & Newell (1961) frequently observed that in conditions of oxygen deficiency (e.g. less than 1 mg O2/l) Macoma balthica (as Macoma balthica) moved upwards to fully expose itself on the surface of the sand. Specimens lay on their side with the foot and siphons retracted but with valves gaping slightly allowing the mantle edge to be brought into full contact with the more oxygenated surface water lying between sand ripples. In addition, Macoma balthica was observed under laboratory conditions to extend its siphons upwards out of the sand into the overlying water when water was slowly deoxygenated with a stream of nitrogen. The lower the oxygen concentration became the further the siphons extended. Dries & Theede (1974) reported the following LT50 (medial lethal time) values for Macoma balthica maintained in anoxic conditions: 50 - 70 days at 5°C, 30 days at 10°C, 25 days at 15°C and 11 days at 20°C. Theede (1984) reported that the ability of Macoma balthica to resist extreme oxygen deficiency was mainly due to cellular mechanisms. Of considerable importance are sufficient accumulations of reserve compounds e.g. glycogen and the ability to reduce energy requirements for maintenance of life by reducing overall activity (Theede, 1984). Macoma balthica is, therefore very tolerant of hypoxia, although it may react by reducing metabolic activity. Intolerance is, therefore assessed as low. Metabolic function should quickly return to normal when normoxic levels are resumed and so recoverability is recorded as very high. Macoma balthica have been shown experimentally to be able to resist time periods of 9 weeks under algal cover (arising from organic enrichment), their long siphon allowing them to reach oxygenated water (Thiel et al., 1998).

Dense Capitella capitata populations are frequently located in areas with greatly elevated organic content, even though eutrophic sediments are often anoxic and highly sulfidic (Tenore, 1977; Warren, 1977; Tenore & Chesney, 1985; Bridges et al., 1994). The polychaetes Capitella capitata, Pygospio elegans and Scoloplos armiger have all been reported to recolonize habitats following periods of anoxia and hypoxia. Following a period of anoxia in the Bay of Somme (north France) that removed cockles, Pygospio elegans increased rapidly but then decreased as cockle abundance recovered (Desprez et al., 1992; Rybarczyk et al.,1996).

Scoloplos armiger has been described as being present in low oxygen areas and as a dominant species in the recolonization of previously anoxic areas (Pearson & Rosenberg, 1978). Intertidal Scoloplos armiger is, in contrast to subtidal specimens, subject to hypoxia when tidal flats are without oxygenated seawater during low tide (Kruse et al., 2004). Tolerance against hypoxia and sulfide is low (Kruse et al., 2004), and worms may ascend into the oxic layer during low tide (Schoettler & Grieshaber, 1988).

Sensitivity assessment. Decreased oxygen levels, would lead to an alteration in sediment chemistry, including the production of hydrogen sulphides that would alter habitat conditions and is likely to lead to mortality of Cerastoderma edule although the characterizing species are likely to be more tolerant. Based on Theede et al., 1996, the sensitivity of the biotope (based on Cerastoderma edule) is ‘Medium’ as periodic immersion would reoxygenate sediments and exposure is likely to be short-term, limiting mortality. Resilience is assessed as ‘high’ and sensitivity is assessed as ‘Low’.

Nutrient enrichment

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

Evidence

This pressure relates to increased levels of nitrogen, phosphorus and silicon in the marine environment compared to background concentrations.  The benchmark is set at compliance with WFD criteria for good status, based on nitrogen concentration (UKTAG, 2014). 

Changes in the nutrient concentrations (e.g. nitrogen and phosphates) are likely to have indirect rather than direct effects on Cerastoderma edule. Increased levels of nutrients at low level may increase phytoplankton productivity and increase food availability for Cerastoderma edule. However, higher nutrient inputs are associated with eutrophication, resulting in increased oxygen consumption and decreased oxygen concentration. Rosenberg and Loo (1988) suggested that the mass mortalities of Cerastoderma edule observed in Laholm Bay, western Sweden during the 1980s was correlated with increased nutrient levels, and associated decrease in oxygen levels during this period (see oxygenation below). However, no direct causal link was established.

Desprez et al. (1992) implicated a eutrophication-induced plankton bloom as the cause of the decline of Cerastoderma edule populations in the Bay of Somme, France. Prior to the event in 1982, densities were several 1000 / m² but by 1982, this had fallen to just a few hundred individuals / m². By 1987, the cockle population had returned.

Sensitivity assessment. As Cerastoderma edule and other characterizing species in the biotope are not primary producers they are not considered directly sensitive to an increase or decrease in plant nutrients in the water column. Phytoplankton and algal detritus may be utilised as food by this genus but supply is not considered to be affected at the pressure benchmark levels. This species is therefore considered to be ‘Not Sensitive’ to this pressure. Resistance is therefore assessed as ‘High’ and resilience as ‘High’ (by default).

Organic enrichment

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

Evidence

Benthic responses to organic enrichment have been described by Pearson & Rosenberg (1978) and Gray (1981).  Moderate enrichment increases food supply enhancing productivity and abundance. Tidal flats (especially mudflats) can be sensitive to organic enrichment which can result in blooms of opportunistic ephemeral seaweeds such as Enteromorpha spp. These can form dense mats, shading the mud surface and leading to anoxic conditions- altering community structure and reducing diversity and abundance and interference with bird feeding (Simpson, 1997). Macoma balthica have been shown experimentally to be able to resist time periods of 9 weeks under algal clover, their long siphon allowing them to reach oxygenated water although other bivalves decreased in abundance (Thiel et al., 1998). Organic enrichment beneath oyster cultivation trestles and mussel cultivation sites and fish cages has led to community replacement/dominance by Cirratulid, Capitellid and Spionid polychaetes, particularly Manayunkia aesturina in mudflats, that characterize disturbed areas enriched in organic matter (Pearson & Rosenberg 1978, Samuelson 2001, see Bouchet and Saurier 2008 for references for activities). Hydrographic and physical conditions (water depth, currents, bottom substrate type) determine particulate matter deposition at any given location, organic matter accumulation in or on the bottom and resulting changes in oxygen status due to aquaculture, can be highly variable within a small area. Gross effects will lead to anoxic, defaunated sediments which may be covered by sulphur reducing bacteria such as Beggiatoa spp. (Elliott et al. 1998). Diatom density may be reduced by organic enrichment potentially reducing the stability of mudflats (Elliott et al. 1998).

Cerastoderma edule and Pygospio elegans have been categorised through expert judgement and literature review as AMBI Group III- species tolerant to excess organic matter enrichment. These species may occur under normal conditions, but their populations are stimulated by organic enrichment (slight unbalance situations). They are surface deposit feeding species (Borja et al., 2000, validated by Gittenberger & van Loon, 2011). Where high levels of organic enrichment occur, bacterial demand may lead to decreases in oxygen (as assessed below). Eteone longa has been described as tolerant of nutrient enrichment (Pearson & Rosenberg, 1978).  Scoloplos armiger, Eteone longa and Eteone flava have been characterized as AMBI Group III.  Species tolerant to excess organic matter enrichment. These species may occur under normal conditions, but their populations are stimulated by organic enrichment (slight unbalance situations). They tend to be surface deposit feeding species (Borja et al. 2000 and Gittenberger & van Loon 2011).  However, a later review characterized Scoloplos armiger as Group II Species indifferent to enrichment, always present in low densities with non-significant variations with time (from the initial state, to slight unbalance). These include suspension feeders, less selective carnivores and scavengers. They tend to be surface deposit-feeding species (Gittenberger & van Loon, 2011). 

Dense Capitella capitata populations are frequently located in areas with greatly elevated organic content, even though eutrophic sediments are often anoxic and highly sulfidic (Tenore, 1977; Warren, 1977; Tenore & Chesney, 1985; Bridges et al. 1994) e.g. sewage-enriched sediments in Kiel Bay (Gray, 1979).

Studies have also identified Pygospio elegans as a ‘progressive’ species, i.e. one that shows increased abundance under organic enrichment (Leppakoski, 1975, cited in Gray, 1979). In the sewage-enriched sediments of Kiel Bay, P. elegans is the numerical dominant.

Sensitivity assessment.  Areas with significant mud contents are likely to be rich in organic matter and low oxygen penetration coupled with high levels of bacterial activity means sediments anoxic a short distance below the surface. Given their adaptation to these habitat conditions the characterizing Cerastoderma edule and other associated species are not considered sensitive to organic enrichment.  Indeed, some species present e.g. Capitella and Pygospio elegans are typical of enriched and anoxic sediments. The biotope is considered ‘Not sensitive’ to this pressure based on ‘High’ resistance and ‘High’ recovery (by default). 

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 occurs in fine sands and muddy sands (JNCC, 2015). A change to natural or artificial hard substratum would remove this sedimentary biotope and the species. If pockets of fine sediment accumulate in pockets within the substrata then these areas may be re-colonised by species associated with this biotope but these pockets of sediment would not be equivalent to the biotope. Recovery will depend on the re-instatement of suitable habitat.

Sensitivity assessment. Based on the loss of suitable habitat, biotope resistance to this pressure is assessed as ‘None’. Resilience is assessed as ‘Very low’ as the pressure benchmark refers to a permanent change. Biotope sensitivity is, therefore ‘High’.

Physical change (to another sediment type)

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

Evidence

The benchmark for this pressure refers to a change in one Folk class.  The pressure benchmark originally developed by Tillin et al. (2010) used the modified Folk triangle developed by Long (2006) which simplified sediment types into four categories: mud and sandy mud, sand and muddy sand, mixed sediments and coarse sediments.  The change referred to is therefore a change in sediment classification rather than a change in the finer-scale original Folk categories (Folk, 1954).  The change in one Folk class is considered to relate to a change in classification to adjacent categories in the modified Folk triangle (Long, 2006). As this biotope occurs within fine sands and muddy sands (JNCC, 2015), the change at the pressure benchmark refers to a potential change to coarse sediments, mixed sediments, sand and muddy sands or mud.

The particle size of sediments and correlated physical and chemical factors (such as drainage, organic matter content and hydrodynamic regime), is a key determinant of the structure of benthic invertebrate assemblages (Van Hoey et al., 2004; Yates et al., 1993).  Free draining coarse sediments such as shingle and gravels have low levels of water and organic content and cohesion and high levels of abrasion as the particles are moved by wind or water action. Although Hall & Harding (1997) report that Cerastoderma edule are found in stoney gravel this is not an optimal sediment for supporting dense populations and coarse sediment shores do not support many of the associated species found in this biotope. A change to coarse sediments would result in loss of characterizing and associated species, resulting in biotope reclassification. In North America, cultivation of clam species including the Manila clam Tapes philippinarum usually involves some form of habitat modification in the form of adding gravel or gravel and crushed shell over mud and sand beaches, to create a more productive clam habitat (referred to as ‘gravelled clam plots’). Such habitat modifications lead to alterations in the local environment and consequently faunal composition. Simenstad & Fresh (1995, cited in Kaiser & Beadman, 2002) reported that the application of gravel to intertidal sediments resulted in a shift from a polychaete to a bivalve and nemertean dominated community, but emphasised that changes are likely to be site-specific.

Infauna can be affected by changes in sediment as many are adapted to burrow through certain grades of sediment (Trueman & Ansell, 1969), decreased fine fractions will reduce habitat suitability for species that maintain permanent burrows. Changes in sedimentary features may also influence the proportions of suspension and deposit feeding animals (Sanders, 1968), with deposit feeders favoured by increases in the proportion of silts and clays.

A study in the Dutch Wadden Sea showed that suction-dredging for cockles (Cerastoderma edule) led to a significant long-term reduction in settlement and stocks of the target bivalve species (Piersma et al., 2001). Analysis of sediment characteristics before and after dredging showed an increase in median grain size and a reduction of silt content, and that these changes were most pronounced in the area dredged for cockles. Sediment characteristics only returned to pre-impact conditions 8-11 years after the suction dredging. The authors concluded that suction dredging of Cerastoderma edule had long lasting effects on the recruitment of bivalves (particularly the target species Cerastoderma edule, but also Macoma balthica) in sandy parts of the Wadden Sea basin. Initial sediment reworking by suction dredging especially during autumn storms) probably caused loss of fine silts and then negative feedback processes appeared to follow that prevented the accumulation of fine-grained sediments conducive to bivalve settlement. 

Macoma balthica thrives in low energy environments such as estuaries (Tebble, 1976) where the substratum has a high proportion of fine sediment. Green (1968) recorded that towards the mouth of an estuary where sediments became coarser and cleaner, Macoma balthica was replaced by another tellin species, Tellina tenuis. Kraan et al. (2007) noted that a reduction in fine silts following cockle dredging was believed to have led to decreased recruitment of Macoma balthica.  These effects persisted for over eight years after dredging (Piersma et al., 2001). Newell (1965) (cited in Green, 1968) noted that Macoma balthica populations in the Thames Estuary, UK, were denser where the grade of deposit was finer, possibly due to greater food availability.

Experimental relaying of mussels on intertidal fine sand sediments increased fine sediment proportions and led to colonisation by Capitella capitata (Ragnarsson & Rafaelli, 1999) Experimental studies have shown that Capitella capitata have increased in abundance where there has been a 2-3 cm layer of fine resuspended and re-settled sediment (McCall, 1977).  However the settlement may be due to enhanced food supply rather than the increase in fine sediments alone.

Eteone longa has wide sediment preferences, it would be able to tolerate an increase in coarse sediments within the habitat envelope. The presence of this species on a range of coarse substrata/sediments indicate that it would be able to tolerate (but possibly with population impacts) an increase in sediment coarseness (e.g. where shells and larger sediments accumulate). However, a transition to a fully coarse sediment type is likely to negatively impact this species as the habitat becomes sub-optimal. Degraer et al. (2006) indicate that a change to a very fine sediment would, however, exclude this species.

Pygospio elegans prefers fine sediments such as sand and mud; increased sediment coarseness is likely to render sediments unsuitable for this species. Empirical evidence supporting this view is provided by Bolam (1999) where experimental manipulation of sediments by implanting macroalgae mats led to increased fine sediment fractions (with associated increased organic and water content) which led to the establishment of Pygospio elegans.

Sensitivity assessment. The character of the habitat is largely determined by the sediment type, changes to this would lead to habitat re-classification. The addition of coarse sand particles or fine particles in sufficient quantities would lead to the development of a different habitat type. Changes in sediment characteristics can lead to changes in community structure. An increase in coarse sediments would lead to the development of a community typical of mixed sediments, clean sands and/or gravels depending on the degree of change.  In general, an increase to very coarse sediments may favour some amphipod species rather than Cerastoderma edule, Macoma balthica, and the associated burrowing polychaetes and sessile tube-dwelling polychaetes. This change would alter the character of the biotope present leading to re-classification, biotope resistance is assesed as 'None' and, as the change is permanent, resilience is assessed as 'Very Low'. Biotope sensitivity is therefore 'High'. 

The presence of the characterizing species in muddy sands indicates that sediments with fine fractions provide suitable habitat and the characterizing and associated species are also found in mud habitats (e.g. Cerastoderma edule, Capitella sp., Pygospio elegans, Eteone sp.). The majority of the species were therefore considered to have ‘High’ resistance to a change to a mud sediment. However, as mudflat habitats are more suitable for deposit feeders than suspension feeders, Cerastoderma edule was considered likely to experience a reduction in habitat suitability following a change in sediment type, a reduced abundance of this species is likely to facilitate colonization by other species typically associated with mud habitats, resulting in a change in assemblage structure and biotope reclassification. Hence, resistance is assessed as 'None'. Recovery will depend on the degree of effect and site specific habitat forming processes, including sediment supply and hydrodynamics. On many shores, areas of different sediment type are found and the extent and location of these may be fairly dynamic, biotope resilience is, however, assessed as ‘Very low’ as the change at the pressure benchmark is considered to be permanent. Sensitivity was, therefore, assessed as 'High'.

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

Sedimentary communities are likely to be highly intolerant of substratum removal, which will lead to partial or complete defaunation, expose underlying sediment which may be anoxic and/or of a different character or bedrock and lead to changes in the topography of the area (Dernie et al., 2003). Any remaining species, given their new position at the sediment / water interface, may be exposed to conditions to which they are not suited, i.e. unfavourable conditions. Recovery by infilling will depend on local factors including the mobility of sediments, sediment supply, hydrodynamics and the spatial scale of the area affected (Van Hoey et al. 2008).

The extraction of sediment would remove the characterizing species and all associated species present, including Cerastoderma edule, which is found to a depth of 5 cm (Tebble, 1976)  and Nephtyid species and other polychaetes, such as Scoloplos armiger and Pygospio elegans that burrow between 5 and 20 cm into the sediment (Sch?ttler,1982; Pedersen, 1991; Kruse et al., 2004).   Undamaged individuals of Cerastoderma edule displaced to the sediment surface may survive and re-bury (Coffen-Smout & Rees, 1999). 

Direct evidence of recovery by Macoma balthica following substratum loss is given by Bonsdorff (1984).  Bonsdorff (1984) studied the recovery of a Macoma balthica (as Macoma balthica) population in a shallow, brackish bay in SW Finland following the removal of the substratum by dredging in the summer of 1976. Recolonization of the dredged area by Macoma balthica began immediately after the disturbance to the sediment and by November 1976, the Macoma balthica population had recovered to 51 individuals/m². One year later there was no detectable difference in the Macoma balthica population between the recently dredged area and a reference area elsewhere in the bay. In 1976, 2 generations could be detected in the newly established population indicating that active immigration of adults was occurring in parallel to larval settlement. In 1977, up to 6 generations were identified, giving further evidence of active immigration to the dredged area.

Sensitivity assessment. Extraction of 30 cm of sediment will remove the characterizing biological component of the biotope and sediments. The resistance of the habitat to extraction is assessed as ‘None’ as sediment is removed: the depth of remaining sediments and their character will be site-specific. Recovery will depend on local factors including hydrodynamics, sediment supply and sediment mobility and the spatial scale affected. Resilience is assessed as ‘Medium’ as sediment infilling may be rapid in intertidal areas, however, recruitment of the characterizing Cerastoderma edule is episodic (see resilience section). Biotope sensitivity is therefore assessed as 'Medium'. If sediments do not return to the previous condition, larval recolonization may be inhibited (see physical change pressures).

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

Muddy sand sediments, in general, tend to be cohesive although high levels of water content will reduce this and destabilise sediments. Sediment cohesion provides some sediment stabilisation to resist erosion following surface disturbance. Species associated with muddy sands/sandy muds are infaunal and hence have some protection against surface disturbance, although tubes of sedentary polychaetes, such as Pygospio elegans, may project above the sediment surface and damage to these would require repair. Cerastoderma edule has short siphons and requires contact with the surface for respiration and feeding.  Surface compaction can collapse burrows and reduce the pore space between particles, decreasing penetrability and reducing stability and oxygen content (Sheehan, 2007).  Trampling (3 times a week for 1 month) associated with bait digging reduced the abundance and diversity of infauna (Sheehan, 2007; intertidal muds and sands). However, Cooke et al .(2002) found that trampling associated with bait digging had little effect on infaunal species composition (intertidal muddy sands).

Chandrasekara and Frid (1996; cited in Tyler-Walters & Arnold, 2008; who inferred the community as intertidal mud from the communities present) found that along a pathway heavily used for five summer months (ca 50 individuals a day) some species (e.g. Capitella capitata and Scoloplos armiger) reduced in abundance while others increased in abundance, probably due to rapid recruitment and growth of more opportunistic species, even though their population experienced mortality. Recovery took place within 5-6 months. Juveniles and adults of Scoloplos armiger stay permanently below the sediment surface and freely move without establishing burrows. While juveniles are only found a few millimeters below the sediment surface, adults may retreat to 10 cm depth or more (Reise, 1979; Kruse et al., 2004) and are likely to be more protected. The egg cocoons are laid on the surface and hatching time is 2-3 weeks during which these are vulnerable to surface abrasion.

Rossi et al. (2007) conducted experimental trampling on a mudflat (5 people, 3-5 hours, twice a month between March and September). Mobile fauna were not affected; however, the abundance of adult Cerastoderma edule was sharply reduced, probably due to the trampling directly killing or burying the animals, resulting in asphyxia. However, no effect was observed on small (<12 mm) individuals of Cerastoderma edule. The authors suggested that this was because the experiment was conducted in the reproductive season for these species and hence there were juveniles present in the water column to replace individuals displaced by trampling. The lack of observed effect was therefore due to continuous recruitment and replacement of impacted individuals.

Sensitivity assessment. Abrasion at the surface is likely to damage a proportion of the population shallow buried bivalves (Cerastoderma edule and Macoma balthica) and soft-bodied species that live on or very close to the surface (Pygospio elegans and Capitella capitella). The level of damage and mortality will depend on the force exerted. Biotope resistance is assessed as ‘Medium’ and resilience is assessed as ‘High’ so that biotope sensitivity is therefore assessed as ‘Low’

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

In contrast to rocky shores, few soft sediment fauna are found on the sediment surface at low tide. As a consequence, harvesting of soft sediment fauna requires the physical disturbance of the substratum. Moreover, these habitats tend to extend over large areas which, coupled with their low topography and the structure of the substratum, makes them amenable to extensive mechanical harvesting (Kaiser et al., 2001). Towed demersal gears, such as beam trawls, otter trawls, scallop dredges, could be deployed in intertidal sandy and muddy habitats depending on the tidal regime and the morphology of the coastline (Hall et al., 2008). Due to commercial interest and the accessibility of intertidal areas, a number of academic studies have assessed the effects of these fisheries, including the impact of sediment disturbance on the species found within this biotope. This assessment is divided into three sections; considering impacts on the key characterizing Cerastoderma edule; associated species and the sedimentary habitat. Changes to sediment are also relevant to the physical change assessments and the evidence for impacts of substratum changes and the impact on the biotope is considered more fully in that section.

Impacts on Cerastoderma edule.

In the Burry Inlet, Wales, intertidal tractor towed cockle harvesting led mechanical cockle harvesting in muddy sand reduced the abundance of Cerastoderma edule by ca 34%. Populations of Cerastoderma edule had not recovered their original abundance after 174 days (Ferns et al. 2000). Hall and Harding (1997) studied the effect of suction and tractor dredging for cockles on non-target benthic fauna in the Solway Firth, Scotland where sediments contained 60-90% silt/clay in the more sheltered areas. The results showed that suction dredging resulted in significantly lower mean species numbers (by up to 30%) and mean numbers of individuals (up to 50%) and in the abundance of 3 of the 5 dominant species. The faunal structure of the dredged plots recovered (i.e. approached that of the undisturbed control plots) by 56 days. The results of the tractor dredge experiments showed fewer effects than the suction dredging (no significant effect on the number of species or individuals). The authors concluded that mechanical harvesting methods imposed high levels of mortality on non-target benthic fauna but that the recovery of disturbed sites was rapid and that the overall effects on populations were low. Although the results suggested that tractor dredging had less impact than suction dredging the authors proposed this may have been due to differences in the timing of the experiments (May-July suction dredging; July-September tractor dredging).They concluded that although significant mortality of Cerastoderma edule and other infauna occurred, recovery was rapid and the overall effects on populations were low. Hall & Harding (1997) found that abundance had returned to control levels within about 56 days and Moore (1991) also suggested that recovery was rapid. Rostron (1995) carried out experimental dredging of sandflats with mechanical cockle dredge. Two distinct sites were sampled; Site A: poorly sorted fine sand with small pools and Arenicola marina casts with some algal growth, and Site B: well sorted fairly coarse sand, surface sediment well drained and rippled as a result of wave activity. At both sites, Cerastoderma edule reduced after dredging but recovery was rapid at Site B (no difference between control and experimental plots after 14 days), whilst at Site A significant reduction in numbers compared with the control were still apparent up to six months post-dredging.

With respect to displacement, cockles are capable of burrowing rapidly into the substratum and >50% burrowed into the substratum within 1 hour in experimental trials (Coffen-Smout & Rees, 1999), although this rate was inhibited by prior disturbance. Brock (1979) reported that 80% began to burrow within 60 min and 50% had successfully burrowed into sediment within 60 min. He also noted that young cockles could burrow quickly, and were nearly buried within 5 min. Hand-raking for cockles was shown not to influence the re-burial rate of cockles in Strangford Lough, Northern Ireland (McLaughlin et al. 2007).

Impacts on associated species

Experiments found that suction dredging to remove cockles led to a decline in associated species richness and species abundance (Hall & Harding, 1998). In contrast, tractor dredging did not lead to significant, observable effects on non-target species. Recovery was tracked following the disturbance, after 56 days there was little difference between dredge and control sites. This rapid recovery coincided with annual recruitment supporting recovery (Hall & Harding, 1998). Several studies have assessed the impact of cockle dredging on non-target species including Macoma balthica. Piersma et al. (2001) showed that after suction dredging for cockles (Cerastoderma edule) in the Dutch Wadden Sea, the abundance of Macoma balthica declined for eight years  Declines of bivalve stocks were caused by low rates of settlement in the fished areas. Hiddink (2003) also reported a significant negative effect of cockle dredging on the density of 0-group Macoma balthica), which persisted for one year after dredging, likely due to the habitat being less suitable following dredging. Kraan et al. (2007) also showed that the deep disturbance from cockle dredging led to decreased densities of Macoma balthica on intertidal mudflats flats (sand and muddy sand sediment) in the Dutch Wadden Sea.

Bergman and Hup (1992) found that worm species (including Scoloplos armiger) showed no change in total density after trawling a subtidal habitat. Conversely, a later study by Bergman and Santbrink (2000) found that the direct mortality of Scoloplos armiger from a single passage of a beam trawl in subtidal silty grounds was 18% of the population. Rostron (1995) undertook experimental dredging of sandflats with a mechanical cockle dredger, including a site comprised of stable, poorly sorted fine sands with small pools and Arenicola marina casts with some algal growths. At this site, post-dredging Scoloplos armiger had disappeared from some dredged plots. Ferns et al. (2000) used a tractor-towed cockle harvester, to extract cockles from intertidal plots of muddy sand and clean sand, to investigate the effects on non-target organisms; 31% of the population of Scoloplos armiger (initial density of 120 per m2) were removed. Populations of Scoloplos armiger remained significantly depleted in the area of muddy sand for more than 50 days after harvesting. Ball et al. (2000) found that species including Scoloplos armiger showed a significant decrease in abundance of between 56-27% after 16 months of otter trawling at a previously unfished Scottish sea loch. Chandrasekara and Frid (1996, cited in Tyler-Walters & Arnold, 2008) found that along a pathway heavily used for five summer months (ca. 50 individuals day-1), Scoloplos armiger reduced in abundance. Recovery took place within 5-6 months. These studies suggest that Scoloplos armiger is likely to be impacted by sediment disturbance and that recovery to previous densities may require more than two years.

A number of studies have found that the abundance of the polychaete Pygospio elegans is reduced by simulated cockle dredging (Hall & Harding, 1998; Moore, 1990; Ferns et al., 2000; Rostron, 1995).  Ferns et al. (2000) found that tractor towed cockle harvesting removed 83% of Pygospio elegans (initial density 1850/ m²).  In muddy sand habitats, Pygospio elegans had not recovered to the original abundance after 174 days (Ferns et al., 2000). Rostron (1995) also found that Pygospio elegans had not recovered to pre-dredging numbers after six months. Conversely, Hall & Harding, (1998) found that abundance of Pygospio elegans increased significantly over 56 days  following suction dredging.  Pygospio elegans inhabits a fragile tube that projects above the sediment surface and is probably more vulnerable to physical disturbance and abrasion than other, more deeply buried, infaunal species.

Rees, 1978, (cited in Hiscock et al., 2002), assessed pipe-laying activities. The pipe was laid in a trench dug by excavators and the spoil from the trenching was then used to bury the pipe. The trenching severely disturbed a narrow zone, but a zone some 50 m wide on each side of the pipeline was also disturbed by the passage of vehicles. The tracked vehicles damaged and exposed shallow-burrowing species such as Cerastoderma edule and Macoma balthica, which were then preyed upon by birds. During the construction period, the disturbed zone was continually re-populated by mobile organisms, such as the mud snail Hydrobia ulvae. Post-disturbance recolonisation was rapid. Several species, including the polychaetes, Eteone longa, and Scoloplos armiger were recruited preferentially to the disturbed area.

Impacts on sediment

Tractor dredging leaves visible tracks in the sediment, which can act as lines for erosion and accelerate erosion of the sediment (Moore, 1991; Gubbay & Knapman, 1999). In most cases, the subsequent settlement was good especially in areas of previously high population density; however, Franklin and Pickett (1978) noted that subsequent spat survival was markedly reduced.  Hall & Harding, (1998), assessed the effects of tractor towed cockle dredgers on sediment erodibility. Effects were short-term, with dredged sediments having greater erodibility (lower shear stress) following dredging which increased over 48 hours back to the levels observed in the undredged plots. Cotter et al., (1997) also noted that dredge tracks not clearly visible after 1 day, demonstrating rapid infilling.

Sensitivity assessment. The available evidence indicates that small patches of physical disturbance are likely to be in-filled by adult cockle movement, large patches will recover through larval recruitment, which again is subject to many factors, and may be improved by the removal of adult cockles. Biotope resistance is assessed as ‘Low’ based on loss of characterizing species Cerastoderma edule and associated species. Resilience is assessed as ‘Medium’ to take account of recruitment variability and return of normal age structure. Sensitivity is therefore categorized as ‘Medium’.

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

Increasing total particulate concentrations have been shown to decrease clearance rates and increase pseudofaeces production in Cerastoderma edule (Navarro et al. 1992; Navarro & Widdows, 1997). Filtration rates increased with particulate concentration until 300 mg/l at which concentration filtration rates abruptly declined. Pseudofaeces production was triggered by concentrations of total particulate matter of 1.5 mg/l (Navarro et al., 1992) or 4.8 mg/l (Navarro & Widdows, 1997). However, the absorption efficiency remained independent of particulate concentration over a large range but reduced at concentrations above 250 mg/l (Navarro & Widdows, 1997). Navarro and Widdows (1997) concluded that Cerastoderma edule was well adapted to living in turbid environments such as intertidal mudflats. Increased siltation and suspended sediment concentration result in increased pseudofaeces production and concomitant loss of energy and carbon as mucus. Therefore, Cerastoderma edule probably has a low intolerance to increased suspended sediment.

Increasing turbidity may reduce phytoplankton productivity and hence decrease food availability, however, Cerastoderma edule is capable of ingesting organic seston and is adapted to life in sedimentary and estuarine conditions where turbidity is high (Navarro & Widdows, 1997). Therefore, Cerastoderma edule is probably tolerant to changes in turbidity (Tyler-Walters, 2007).

A decrease in turbidity and hence increased light penetration may result in increased phytoplankton production and hence increased food availability for suspension feeders, including Cerastoderma edule. Therefore, reduced turbidity may be beneficial. In areas of high suspended sediment, a decrease may result in improved condition and recruitment due to a reduction in the clogging of filtration apparatus of suspension feeders and an increase in the relative proportion of organic particulates. However, a decrease in suspended organic particles in some areas may reduce food availability resulting in lower growth or reduced energy for reproduction. Infauna not directly affected but may be indirectly affected by changes in sediment composition from increased deposition or reduction in biodeposition from Cerastoderma edule from reduced clearance.

Macoma balthica is known to practice two alternative modes of feeding. It either holds its feeding organ, the siphon, at a fixed position just above the sediment surface to filter out food particles suspended in the overlying water, or extends and moves its siphon around on the sediment above it to vacuum up deposited food particles (Peterson & Skilleter, 1994). Facultative switching between the modes of feeding in Macoma balthica is directly affected by food availability in the over-lying water (Lin & Hines, 1994). In turn, changes in feeding mode from suspension to deposit feeding directly affects burial depth. In the laboratory, Lin & Hines (1994) observed specimens of Macoma balthica kept in estuarine water supplemented with 75 µg/l of algae to maintain a deeper burial position whilst suspension feeding, than those without an enhanced diet who deposit fed. Thus, an increase of material in suspension will favour suspension feeding by Macoma balthica and indirectly reduce its vulnerability to lethal and sub-lethal siphon browsing by fish and decapods. Macoma balthica is therefore assessed as 'tolerant' with the potential for growth and reproduction to be enhanced by the increased food supply.

Sensitivity assessment. A decrease in turbidity and hence increased light penetration may result in increased phytoplankton production and hence increased food availability for suspension feeders, including Cerastoderma edule. Therefore, reduced turbidity may be beneficial. In areas of high suspended sediment, a decrease may result in improved condition and recruitment due to a reduction in the clogging of filtration apparatus of suspension feeders and an increase in the relative proportion of organic particulates. However, a decrease in suspended organic particles in some areas may reduce food availability for deposit feeders resulting in lower growth or reduced energy for reproduction. Where increased turbidity results from organic particles then subsequent deposition may enhance food supply for deposit feeders within the biotope such as Macoma balthica and deposit feeding polychaetes. Alternatively, if turbidity results from an increase in suspended inorganic particles then energetic costs may be imposed on these species as sorting and feeding becomes less efficient reducing growth rates and reproductive success. Lethal effects are considered unlikely given the occurrence of Cerastoderma edule and other associated species in estuaries where turbidity is frequently high from suspended organic and inorganic matter. Resistance and resilience are therefore assessed as 'High' and the biotope is conisdered to be 'Not sensitive'.

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

Cerastoderma edule has short siphons and needs to keep in contact with the surface of the sediment. Richardson et al. (1993) reported that they burrow quickly to the surface if covered by 2 cm of sediment (under laboratory or field conditions) when emersed (45% of cockles emerged onto the surface in light and 60% in darkness). In light the cockles quickly re-burrow, however, in darkness they move across the substratum, partly to increase the distance between neighbours. Richardson et al. (1993) suggested that surface movement in darkness might be a response to coverage from siltation.

Bait digging (for large polychaete worms) disturbs the sediment down to a depth of 30cm (Jackson & James, 1979) and results in repositioning of species when the extracted sediment is placed back in holes or smothering where sediment is piled on the surface. Intensification of bait digging on intertidal flats on the north Norfolk coast for lugworm (Arenicola marina) and ragworm (Hediste diversicolor) was associated with declines in the Cerastoderma edule populations (Jackson & James, 1979). Experimental simulation of bait digging (sediment dug over to a depth of 30cm with a garden fork) led to high mortalities of cockles in dug areas rather than undug areas (48% mortality in 9 days to a maximum of 85% after 11 days) probably due to smothering (Jackson & James, 1979). The observation was tested experimentally in the laboratory by burying 3 size-classes of cockles at 0, 5 or 10cm depth in a mix of oxidated and deeper anoxic sands (mixed as a ratio of 3:1) was used as the sediment. Movements were recorded after 24, 48 and 72 hours. When buried to 5 cm depth most cockles returned to the surface but few were able to reposition to the surface if buried at 10cm depth. None had died after 72 hours. Additional burial experiments under 10 cm of sediment assessed movement and survival after 3, 6 and 9 days in two sediment types (a mix of surface mud and sand in two ratios 9:1 and 1:9).  The movement towards the surface was slower in the predominantly muddy sediment and all cockles died between 3 and 6 days. Substantial mortality resulted in the predominantly sandy mixture although some cockles were able to move towards the surface and survive for 9 days.

Gam et al. (2010) compared population dynamics and secondary production of Cerastoderma edule between Merja Zerga on the Moroccan Atlantic coast (close to the species southerly limit) and Arcachon Bay on the French Atlantic coast. During their study of recruitment in January 2007, mass mortalities were observed in both adult and juvenile cockles and this was attributed to high sand bank displacements in the previous year, which partly covered and smothered the cockle population.

Macoma balthica is able to burrow both vertically and horizontally through the substratum. It is likely that Macoma balthica is not sensitive to smothering by a layer of sediment 5 cm thick as it is a mobile species able to burrow upwards and surface from a depth of 5 - 6 cm (Brafield & Newell, 1961; Brafield, 1963; Stekoll et al., 1980). Turk and Risk (1981) investigated the effect of experimentally induced sedimentation (through fences and boxes that induced sediment deposition on intertidal mudflats in the Bay of Fundy), of 1-3.5cm at a rate of 1.9-10.2 cm/month. The results showed that Macoma balthica was generally unaffected.

The associated species Pygospio elegans is limited by high sedimentation rates (Nugues et al., 1996) and the species does not appear to be well adapted to oyster culture areas where there are high rates of accumulation of faeces and pseudo faeces (Sornin et al., 1983; Deslous-Paoli et al., 1992; Mitchell, 2006 and Bouchet & Sauriau 2008).  Pygospio elegans is known to decline in areas following re-deposition of very fine particulate matter (Rhoads & Young, 1971; Brenchley, 1981). Experimental relaying of mussels on intertidal fine sands led to the absence of Pygospio elegans compared to adjacent control plots. The increase in fine sediment fraction from increased sediment deposition and biodeposition alongside possible organic enrichment and decline in sediment oxygen levels was thought to account for this (Ragnarsson & Rafaelli, 1999).

Mobile and/or burrowing species (including molluscs and polychaetes such as Hydrobia ulvae, Eteone longa and Scoloplos armiger) are generally considered to be able to reposition following periodic siltation events or low levels of chronic siltation. Field experiments where 10 cm of sediment were placed on intertidal sediments to investigate the effects of the beneficial use of dredged materials found that the abundance of Hydrobia ulvae had returned to ambient levels within 1 week (Bolam et al. 2004). However, survival depends on several factors. The snail can only burrow up through certain sorts of sediment. If the silt content of the smothering sediment is high and the water content low then it is unlikely that the surface will be regained from 5 cm down. Looser sediment with high water and low silt content can be negotiated quite rapidly. The surface is generally regained within a day. If the surface cannot be regained then Hydrobia ulvae can survive burial for quite extended periods although this is highly temperature dependent. Temperatures of 20^oC result in all individuals dying after 10 days. Survival is much better at lower temperatures. It is thought that oxygen stress is the cause of mortality (Jackson, 2000).

Sensitivity assessment. Biotope resistance based on the characterizing Cerastoderma edule is assessed as having ‘Medium’ resistance to siltation, (as many would be able to survive and re-emerge from a 5cm depth of sediment). Resilience is assessed as ‘High’ based on adult migration and repopulation by larvae. Many of the associated species are also likely to reposition although Pygospio elegans may be more sensitive.

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

Cerastoderma edule has short siphons and needs to keep in contact with the surface of the sediment. Bait digging (for large polychaete worms) disturbs the sediment down to a depth of 30 cm (Jackson & James, 1979) and leads to repositioning within sediment or burial from piled sediments. Intensification of bait digging on intertidal flats on the north Norfolk coast for lugworm (Arenicola marina) and ragworm (Hediste diversicolor) was associated with declines in the Cerastoderma edule populations (Jackson & James, 1979). Experimental simulation of bait digging (sediment dug over to a depth of 30 cm with a garden fork) led to high mortalities of cockles in dug areas rather than undug areas (48% mortality in 9 days to a maximum of 85% after 11 days) probably due to smothering (Jackson & James, 1979). The observation was texted experimentally in the laboratory by burying 3 size-classes of cockles at 0, 5 or 10 cm depth in a mix of oxidated and deeper anoxic sands (mixed as a ratio of 3:1) was used as the sediment. Movements were recorded after 24, 48 and 72 hours. When buried to 5 cm depth most cockles returned to the surface but few were able to reposition to the surface if buried at 10cm depth. None had died after 72 hours. Additional burial experiments under 10 cm of sediment assessed movement and survival after 3, 6 and 9 days in two sediment types (a mix of surface mud and sand in two ratios 9:1 and 1:9).  The movement towards the surface was slower in the predominantly muddy sediment and all cockles died between 3 and 6 days. Substantial mortality resulted in the predominantly sandy mixture although some cockles were able to move towards the surface and survive for 9 days.

Maurer et al. (1986) studied the effects of dredged material on the vertical migration and mortality of four species of benthic invertebrates (including two polychaetes) and reported that the intolerance of species to smothering was influenced by the nature of the sediment. They predicted that some individuals of both the polychaete species studied (Nereis succinea and Scoloplos fragilis) would be capable of vertical migration through 0.9 m of sediment if that sediment was indigenous to their usual habitat (Marshall, 2008).

Field experiments where 10 cm of sediment were placed on intertidal sediments to investigate the effects of the beneficial use of dredged materials found that the abundance of Hydrobia ulvae had returned to ambient levels within 1 week (Bolam et al. 2004). It is not clear whether this species could reposition after 30cm of sediment were placed on sediments.

Sensitivity assessment. The addition of 30 cm of sediment would prevent Cerastoderma edule and Macoma balthica from extending siphons to the surface. It is unlikely that these species could emerge from this depth of sediment although some individuals may survive and sediment may be rapidly removed by tide and wave action. It is likely, however, that there would be considerable mortality of the characterizing Cerastoderma edule and biotope sensitivity is based on this species. Resistance is assessed as ‘Low’ and resilience as ‘Medium’ (based on episodic recruitment). Sensitivity is, therefore, assessed as ‘Medium’. The sensitivity of the associated species is unclear. Although some polychaetes may be able to reposition following sedimentation at the pressure benchmark this will depend on the characteristics of the overburden and sedentary species such as Pygospio elegans are likely to suffer high levels of mortality.

Litter

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

Evidence

Not assessed.

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.

Introduction of light or shading

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

Evidence

The key characterizing and associated species do not photosynthesize and are unlikely to be directly affected by shading or increased light levels.  The abundance and production of microphytobenthos in sediments may be impacted by shading and this may have indirect effects on secondary production by animals that feed on these. The key characterizing species Cerastoderma edule feeds on suspended seston and is unlikely to be directly affected by localised changes in microphytobenthos production.

Cerastoderma edule carries about 60 eyes on the sensory siphonal tentacles (Barber & Wright 1968). The basic response to light in bivalves is defensive with responses including digging, closing of valves and siphonal withdrawal (Morton, 2008). Changes in light levels may also simulate other behavioural responses and emergence of cockles in response to darkness has been observed (Richardson et al., 1993). The polychaetes found within the biotope including Eteone longa, Capitella capitata and others contain photoreceptors (Purschke et al., 2006) and are likely to perceive changes in light levels.

Light levels may act as cues for reproduction (although temperature also regulates reproduction for many species) supporting synchronised spawning for species with external fertilisation.  No evidence was found to suggest that light levels are an important reproductive cue for characterizing and associated species.

Sensitivity assessment. Light penetration into sediments is limited to the surface layers and permanently buried infauna such as Scoloplos armiger are unlikely to be affected by changes in light levels. The characterizing Cerastoderma edule and other species present can perceive light but the effects of changes in light level and shading or the duration of light and darkness are not clear. As It is considered unlikely that changes in light levels would have significant effects on the key and associated species, biotope resistance is assessed as ‘High’ and resilience as ‘High’ (by default) and the biotope is considered to be ‘Not sensitive’.

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 Cerastoderma edule and Macoma balthica 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.  Species that do not have a pelagic larval stage such as Scoloplos armiger  or those that alternate between pelagic and benthic dispersal stages such as Pygospio elegans and Capitella capitata are less likely to be impacted by this pressure. As both the key characterizing species are widely distributed and have larvae capable of long distance transport and long residence times in the water column, 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

No evidence found. As the species characterizing this biotope are not primary producers , have limited visual acuity and inhabit turbid, coastal waters and estuaries where light penetration may be limited the pressure is assessed as 'Not relevant' to this biotope.

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

The key characterizing and associated species within this biotope are not cultivated or translocated. This pressure is therefore considered ‘Not relevant’ to this biotope group.

Due to long distance transport of pelagic larvae populations of the key characterizing species, Cerastoderma edule, may be interconnected and populations are not genetically isolated, with populations such as those at Pembroke showing mixing between British and Irish populations (Coscia et al., 2013). It should be noted that where local hydrodynamics prevent larval transport some genetically isolated populations may occur, as in the Burry Inlet, south Wales (Coscia et al., 2013).

Introduction or spread of invasive non-indigenous species

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

Evidence

Intertidal flats may be colonized by the invasive non-indigenous species Crepidula fornicata and Magallana gigas. The two species have not only attained considerable biomasses from Scandinavian to Mediterranean countries but have also generated ecological consequences such as alterations of benthic habitats and communities, or changes to the food chain (OSPAR, 2009).

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). However, adults are long-lived so 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). It also prefers mudflats with mixed sediment composed of shingle and sand, attaching to whatever hard substrata are available within otherwise unsuitable fine muddy sediment (Spencer et al., 1994; Mckinstry & Jensen, 2013; Tillin et al., 2020).

Magallana gigas has been reported from estuaries growing on intertidal mudflats, sandflats, and other soft sediments (Padilla, 2010; Herbert et al., 2016; Cabral et al., 2020). The settlement of spat on hard substrata within sediments has been observed in the estuaries of the River Dart, Exe, Fal, Fowey, Tamar, Teign, and Yealm in Devon and Cornwall, the Menai Straits, Wales and large estuaries of Lough Swilly, Lough Foyle and the Shannon in Ireland, and the Tagus Estuary in Portugal (Spencer et al., 1994; Kochmann, 2012; Kochmann et al., 2013; Cabral et al., 2020). In Lough Swilly, Lough Foyle and the Shannon, the Pacific oyster was often associated with intertidal mud or sandflats (Kochmann et al., 2013). In contrast, the Pacific oysters were absent from sandflat areas in Poole Harbour (Mckinstry & Jensen, 2013).

Although shorelines comprised of mainly mud were suggested to be unsuitable for spat settlement (Spencer et al., 1994), the presence of smaller hard substrata, such as shells or pebbles, can enable larvae to settle (Tillin et al., 2020). For example, in the River Teign estuary, Pacific oyster settlement was observed on shell-covered ground mainly attached to mussel shells, and occasionally attached to cockles, stones and common periwinkle (Littorina littorea) shells on a mud flat in the estuarine intertidal zone otherwise mainly comprised of sand and mud (Spencer et al., 1994). In addition, the Blue Lagoon on the north shore of Poole Harbour had the highest abundance of oysters on mud mixed with shingle and shell (Mckinstry & Jensen, 2013). Outside of the Blue Lagoon, oysters were also recorded on mixed substrata composed of mud, gravel, and shell (McKinstry & Jensen, 2013). Tillin et al. (2020) concluded that while successful invasions occurred on mudflats, Magallana gigas prefers mixed substrata. Fine mud sediments without hard substrata (such as small stones, gravel, and shell) are unlikely to be suitable (Tillin et al., 2020). The speed of Magallana gigas reef formation on soft substrata seems to be dependent on the amount of hard substrata present, developing quicker once there is a sufficient amount (Troost, 2010). Bergstrom et al. (2021) reported that the presence of Magallana gigas was partially dependent on increasing gravel content up to 15% but remained stable with increasing percentages (measured up to 80%).

In the Wadden Sea, the distribution of Magallana gigas on soft sediment shores can overlap with native bivalve species such as Cerastoderma edule, Macoma balthica and Scrobicularia plana (Troost, 2010; Herbert et al., 2012, 2016). However, these native species are likely to occur at higher shore elevations compared to the lower shore habitats preferred by the Pacific oyster (Troost, 2010; Herbert et al., 2012, 2016). For example, in the Wadden Sea, greater densities of Cerastoderma edule and Macoma balthica were found above the level of Magallana gigas reef development, with initial colonization of the oyster occurring on former mussel bed and cockle shell ridges (Herbert et al., 2012). Troost (2010) suggested that competition for space between Cerastoderma edule and Magallana gigas was likely to occur at locations unsuitable for the cockles. In addition, Pacific oysters have been observed settling on native cockle shell debris within Zostera noltii beds in South Devon and have been found on the lower shore in a cockle dominated habitat (LS.LSa.MuSa.CerPo) in the Tamar-Tavy estuary (Morgan et al., 2021). 

The oyster reefs in the Wadden Sea and Brittany on littoral muddy and sandy habitats formed predominantly at lower tidal levels from Mean Low Water to the shallow subtidal (Herbert et al., 2012, 2016). Pacific oyster spatfall was recorded in the estuarine intertidal zone on areas with hard substrata of stone and shell, particularly between the low water of spring tides and high water of neap tides, such as in the Menai Strait (Spencer et al., 1994). 

At high densities the Pacific oyster reef smothers sediment, provides hard substrata in an otherwise sedimentary environment with additional niches for colonization by other species that require hard substratum (e.g. barnacles), and changes surface roughness and local hydrography (Troost, 2010; Herbert et al., 2012, 2016; Tillin et al., 2020). Lejart & Hily (2011) found the surface available for epibenthic species in the Bay of Brest, increased 4-fold when oysters were present on mud, for every 1 m² of colonized substrata the oyster reef added 3.87 m² of surface area on mud sediment. An increase in available settlement substrata, free of epibiota, could be the reason oyster reefs see an increase in macrofaunal abundance. This can change the community composition and habitat structure in reefs on soft mud sediments, creating new habitats for an increasing abundance of infaunal and epibenthic mobile species (Kochmann et al., 2008; Lejart & Hily, 2011; Zwerschke et al., 2018). Results have shown 38% of species present in the oyster reefs on mud were characteristic of rocky substratum habitats (Lejart & Hily, 2011).

In the Bay of Brest, Pacific oyster reefs had a higher diversity and species richness than surrounding mud habitats, including the mud underneath the reefs, where the population was dominated by carnivores rather than suspension the feeders found on the mudflats (Lejart & Hily, 2011; Herbert et al., 2012). In addition, in muddy habitats around the UK, Ireland and Northern France, macrofaunal diversity increased as Pacific oyster density increased but epifaunal diversity decreased as oyster densities increased (Zwerschke et al., 2018). It was suggested that the decrease in epifaunal diversity was due to the decrease in settlement space and an increase in habitat fragmentation because of dense oyster assemblages (Zwerschke et al., 2018).

Green & Crowe (2014) examined the effects of Magallana gigas density in experimental plots (0.25 m²) in Lough Swilly and Lough Foyle, Ireland. The number of species and species diversity increased with oyster cover on mudflats, depending on site and duration. The assemblage also changed due to the increased abundance of barnacles and bryozoans on the oyster shells and polychaetes within the sediment (Green & Crowe, 2014). Zwerschke et al. (2020) suggested that Pacific oyster beds could replace the ecosystem services provided by native oysters, in areas where native oysters had been lost. Morgan et al. (2021) suggested that the smothering of sediment habitats could prevent fish and bird species from feeding on infauna like worms, molluscs, and crustaceans. Also, the development of tidepools within mixed Pacific oyster and blue mussel reefs in soft sediment intertidal sites has been observed in the Wadden Sea, which can create new microhabitats within the reefs (Weniger et al., 2022).

Pacific oysters have been found to reduce the proportion of fine particles and increase the proportion of large particles in the mud under the reef (Lejart & Hily, 2011). The evidence suggests that Pacific oyster reefs change sediment characteristics, by affecting nutrient cycling and increasing the organic content of sediment, sand-to-silt ratio and levels of porewater ammonium (Kochmann et al., 2008; Padilla, 2010; Wagner et al., 2012 cited in Tillin et al., 2020; Green & Crowe, 2014; Herbert et al., 2012, 2016; Zwerschke et al., 2020; Hansen et al., 2023). Zwerschke et al. (2020) found no significant differences in nutrient cycling rates of native oyster beds or Magallana gigas beds or their associated benthic communities, in experimental plots in Ireland. Persistent changes in the rates of nutrient cycling were driven by the density and presence of oysters (Zwerschke et al., 2020).

The deposition of faeces and pseudo-faeces by Magallana gigas can increase the toxic levels of sulphide in sediments and associated hypoxic sediment conditions, which can reduce photosynthesis and growth in eelgrass (Kelly & Volpe, 2007). Faecal deposition and hypoxia have also been suggested to explain a reduction in species diversity in the sediment underlying high density oyster reefs (Green & Crowe, 2013, 2014; Herbert et al., 2016). However, Lejart & Hily (2011) observed no organic or silt enrichment by Pacific oysters in mud beneath oyster reefs in the Bay of Brest, and no significant difference in the amount of organic matter found in the mud underneath oyster reefs and on bare mud not colonized by the oyster. The biodeposits excreted by the oyster may be washed away by powerful tides and currents seen in the Bay of Brest and the effects of organic enrichment at oyster reefs might be minimal due to wave action (Lejart & Hily, 2011).

The American slipper limpet Crepidula fornicata was introduced to the UK and Europe in the 1870s from the Atlantic coasts of North America with imports of the eastern oyster Crassostrea virginica. It was recorded in Liverpool in 1870 and the Essex coast in 1887-1890. It has spread through expansion and introductions along the full extent of the English Channel and into the European mainland (Blanchard, 1997, 2009; Bohn et al., 2012, 2013a, 2013b, 2015; De Montaudouin et al., 2018; Helmer et al., 2019; Hinz et al., 2011; McNeill et al., 2010; Powell-Jennings & Calloway, 2018; Preston et al., 2020; Stiger-Pouvreau & Thouzeau, 2015).

Crepidula fornicata is recorded from shallow, sheltered bays, lagoons and estuaries or the sheltered sides of islands, in variable salinity (18 to 40) although it prefers ca 30 (Tillin et al., 2020). Larvae require hard substrata for settlement. It prefers muddy gravelly, shell-rich, substrata that include gravel, or shells of other Crepidula, or other species e.g., oysters, and mussels. It is highly gregarious and seeks out adult shells for settlement, forming characteristic ‘stacks’ of adults. But it also recorded in a wide variety of habitats including clean sands, artificial substrata, Sabellaria alveolata reefs and areas subject to moderately strong tidal streams (Blanchard, 1997, 2009; Bohn et al., 2012, 2013a, 2013b, 2015; De Montaudouin et al., 2018; Hinz et al., 2011; Powell-Jennings & Calloway, 2018; Preston et al., 2020; Stiger-Pouvreau & Thouzeau, 2015; Tillin et al., 2020).

High densities of Crepidula fornicata cause ecological impacts on sedimentary habitats. The species can form dense carpets that can smother the seabed in shallow bays, changing and modifying the habitat structure. At high densities, the species physically smothers the sediment, and the resultant build-up of silt, pseudofaeces, and faeces is deposited and trapped within the bed (Tillin et al., 2020, Fitzgerald, 2007, Blanchard, 2009, Stiger-Pouvreau & Thouzeau, 2015). The biodeposition rates of Crepidula are extremely high and once deposited, form an anoxic mud, making the environment suitable for other species, including most infauna (Stiger-Pouvreau & Thouzeau, 2015, Blanchard, 2009). For example, in fine sands, the community is replaced by a reef of slipper limpets, that provide hard substrata for sessile suspension-feeders (e.g., sea squirts, tube worms and fixed shellfish), while mobile carnivorous microfauna occupy species between or within shells, resulting in a homogeneous Crepidula dominated habitat (Blanchard, 2009). Blanchard (2009) suggested the transition occurred and became irreversible at 50% cover of the limpet. De Montaudouin et al. (2018) suggested that homogenization occurred above a threshold of 20-50 Crepidula /m². 

Impacts on the structure of benthic communities will depend on the type of habitat that Crepidula colonizes. De Montaudouin & Sauriau (1999) reported that in muddy sediment dominated by deposit-feeders, species richness, abundance and biomass increased in the presence of high densities of Crepidula (ca 562 to 4772 ind./m²), in the Bay of Marennes-Oléron, presumably because the Crepidula bed provided hard substrata in an otherwise sedimentary habitat. In medium sands, Crepidula density was moderate (330-1300 ind./m²) but there was no significant difference between communities in the presence of Crepidula. Intertidal coarse sediment was less suitable for Crepidula with only moderate or low abundances (11 ind./m²) and its presence did not affect the abundance or diversity of macrofauna. However, there was a higher abundance of suspension–feeders and mobile Crustacea in the absence of Crepidula (De Montaudouin & Sauriau, 1999). The presence of Crepidula as an ecosystem engineer has created a range of new niche habitats, reducing biodiversity as it modifies habitats (Fitzgerald, 2007). De Montaudouin et al. (1999) concluded that Crepidula did not influence macroinvertebrate diversity or density significantly under experimental conditions, on fine sands in Arcachon Bay, France. De Montaudouin et al. (2018) noted that the limpet reef increased the species diversity in the bed, but homogenised diversity compared to areas where the limpets were absent. In the Milford Haven Waterway (MHW), the highest densities of Crepidula were found in areas of sediment with hard substrata, e.g., mixed fine sediment with shell or gravel or both (grain sizes 16-256 mm) but, while Crepidula density increased as gravel cover increased in the subtidal, the reverse was found in the intertidal (Bohn et al., 2015). Bohn et al. (2015) suggested that high densities of Crepidula in high-energy environments were possible in the subtidal but not the intertidal, suggesting the availability of this substratum type is beneficial for its establishment. Hinz et al. (2011) reported a substantial increase in the occurrence of Crepidula off the Isle of Wight, between 1958 and 2006, at a depth of ca 60 m, on hard substrata (gravel, cobbles, and boulders), swept by strong tidal streams. Presumably, Crepidula is more tolerant of tidal flow than the oscillatory flow caused by wave action which may be less suitable (Tillin et al., 2020).

The availability of hard substrata (e.g., gravel) may only restrict initial colonization as higher densities of Crepidula function as substrata for subsequent colonization (Thieltges et al., 2004; Blanchard, 2009). However, Bohn et al. (2015) noted that Crepidula occurred at low density or was absent in areas of homogenous fine sediment and areas dominated by boulders. Bohn et al. (2015) suggested that wave action (exposure) probably prevented the establishment of large numbers of Crepidula in high-energy areas. Blanchard (2009) noted that sandy areas in the Bay of Saint-Mont Michel were not colonized by Crepidula because of surface sand mobility. Thieltges et al. (2003) also noted that storm events removed some clumps of mussels and presumably Crepidula onto tidal flats where they disappeared, which caused their abundance to fluctuate. Similarly, Crepidula was absent from sandy substrata in Swansea Bay but was most abundant in the shelter of the breakwater at the Swansea east site (Powell-Jennings & Calloway, 2018). Powell-Jennings & Calloway (2018) noted that Crepidula is killed by sudden burial and possibly burial due to deposition, which could mitigate Crepidula density. In addition, in the MHW, the highest densities of Crepidula were found in areas of sediment with hard substrata, e.g., mixed fine sediment with shell, or gravel or both but, while Crepidula density increased as gravel cover increased in the subtidal, the reverse was found in the intertidal (Bohn et al., 2015). However, gravel formed the base of most stacks of Crepidula in the intertidal, which suggested that initial colonization occurred on available hard substrata (i.e., gravel) in the absence of adult shells of Crepidula (Bohn et al., 2015).

Crepidula is recorded from the lower intertidal to ca 160 m in depth but it is most common in the shallow subtidal and low water springs (Blanchard, 1997; Thieltges et al., 2003; Bohn et al., 2012, 2015; Hinz et al., 2011; OBIS, 2023; Tillin et al., 2020). Bohn et al. (2012, 2013a, 2013b, 2015) suggested that extreme conditions in intertidal limited its upward distribution due to early post-settlement mortality. It reached its highest densities on the lower shore (below ca 0.7 m) and was absent from the high tidal level (ca 1.8 m) in the MHW (Bohn et al., 2015). Bohn et al. (2013b) noted that Crepidula spat in their experimental intertidal panels suffered high mortality of 78-100% during emersion by low water spring tides. Thieltges et al. (2003) noted that Crepidula abundance at the intertidal to the subtidal transition zone (ca 21/ m²) was significantly higher than in the upper, mid, and lower intertidal ca <3/ m²). Similarly, Diederich & Pechenik (2013) noted that Crepidula densities were not significantly different in the low intertidal (+0.2 m) and shallow subtidal (-1 m) but became lower at +0.4 and were absent above +0.6 m in Bissel Cove, Rhode Island where the mean high water was +1.38 m. They reported that intertidal adults experienced temperatures of ca 42°C, which were 15°C higher than subtidal adults. However, there was no significant difference in the tolerance of subtidal and intertidal adults with a lethal range of 33-37°C after three hours in the laboratory. Diederich & Pechenik (2013) suggested that adult Crepidula were living close to their upper thermal limit in Rhode Island and would be driven into the subtidal due to climate change. Diederich et al. (2015) reported that most juvenile Crepidula died after aerial exposure under laboratory conditions (20°C, 75% relative humidity), while adults from the intertidal and subtidal survived (26°C, 75% relative humidity). Franklin et al. (2023) noted that the body mass index of adult Crepidula did not decrease significantly in winter months in New Hampshire, USA, but did decrease in spring and summer, probably due to its investment in reproduction. 

The density of Crepidula populations in northern Europe (Germany, Denmark, and Norway) was significantly lower (ca <100/ m2) than in southern waters. Thieltges et al. (2004) reported that the population of Crepidula was affected strongly by cold winters in the Wadden Sea. The winters of 2001 and 2003 resulted in ca 56-64% mortality of intertidal Crepidula and up to 97% on one mussel bed, compared to only 11-14% in southern areas without frost. Crepidula almost vanished from the Wadden Sea after the 1978/79 winter and took ten years to recover due to moderate winters which regularly affected the population. Similarly, 25% mortality was observed in Crepidula populations on the south coast of the UK after the extreme 1962/63 winter (Crisp, 1964, Bohn et al., 2012). Thieltges et al. (2003) suggested that global warming may allow Crepidula populations to become more abundant in northern Europe.

The Manila clam (Tapes philippinarium), which was introduced to Poole Harbour for aquaculture in 1998, has become a naturalised population on the intertidal mudflats (occurring at densities of 60 clams/m² in some locations within the harbour (Jensen et al. 2007, cited in Caldow et al. 2007).  Densities of Cerastoderma edule and Abra tenuis have increased since the introduction of the Manila clam although the abundance of Scrobicularia plana and Macoma balthica declined (Caldow et al., 2005), although the decline of these species may have been caused by tri-butyl tin pollution (Langston et al. 2003) and may have facilitated the naturalization of the Manila clam. The burrowing lifestyle of Eteone longa and other infaunal polychaetes may confer some protection from changes to the sediment surface and may provide some new habitat (as this species has been found among oyster banks). The predatory veined whelk (Rapana venosa) and Hemigrapsus takinei are not established in the UK (although Hemigrapsus takinei has been recorded at two locations) could become significant predators of Cerastoderma edule and other species associated with the biotope in the future.

Sensitivity assessment. Intertidal muddy sands may be exposed to invasive species which can alter the character of the habitat (primarily Crepidula fornicata at the sublittoral fringe and Magallana gigas), leading to re-classification of this biotope. The above evidence suggests that this biotope is unsuitable for the colonization of Crepidula fornicata due to a lack of gravel, shells, or any other hard substrata used for larvae settlement (Tillin et al., 2020), especially in moderately exposed examples in which storms may mobilise the sediment (JNCC, 2022). Despite the extremely sheltered examples of the biotope that would otherwise be suitable for Crepidula, the mobility of the sediment is unsuitable and makes it unlikely for Crepidula to become established. There may be higher densities of Crepidula in the lower shore examples of the biotope, but the densities may be lower in the mid-shore, and it may be absent from the upper shore due to the unsuitable extreme conditions in the intertidal zone preventing Crepidula post-settlement recruitment and mitigating colonization (Bohn et al. 2015). In addition, the reduced salinity levels in this biotope might prevent colonization at high densities, because the majority of evidence records of Crepidula occur in salinities from 30-35 psu (OBIS, 2023). However, the biotope is recorded in the Wash, which already harbours Crepidula in high densities and at low densities on Cerastoderma edule beds (lays) (Quinn, 2018). Quinn (2018) suggested that sediment mobility in the Wash may restrict its abundance on cockle lays. Therefore, resistance to colonization by Crepidula is assessed as 'Medium', as a worst-case scenario. Resilience is assessed as 'Very low' as it would require the removal of Crepidula, probably by artificial means. Hence, sensitivity is assessed as 'Medium'. The confidence in the assessment is 'Low' because the sensitivity of this biotope to Crepidula is potentially site-specific, there is a risk of its introduction by artificial means, and there is a lack of direct evidence of Crepidula being reported to occur in this biotope.

The presence of cockle shells in this biotope could provide suitable hard substrata for settlement by Magallana gigas because it was reported to colonize cockle-shell ridges in the Wadden Sea (Herbert et al., 2012). Magallana gigas has been found to colonize examples of this biotope in the Tamar-Tavy estuary (Morgan et al., 2021).  The mid-shore and upper-shore extent of this biotope is not suitable for colonization of the Pacific oyster, which is found predominantly at the Mean Low Water levels to shallow subtidal (Herbert et al., 2012, 2016).  However, the oyster could colonize the lower-shore extent or examples of the biotope in higher densities. The distribution of Magallana gigas can overlap with Cerastoderma edule and other native bivalve species (Troost, 2010; Herbert et al., 2012, 2016), However, Cerastoderma edule is generally found at higher shore elevations compared to the lower shore habitats preferred by the Pacific oyster, with greater densities of Cerastoderma edule found above the level of Magallana gigas reef development (Troost, 2010; Herbert et al., 2012, 2016). Therefore, resistance to colonization by Magallana gigas is assessed as 'Medium' to represent colonization of the lower shore extent of this biotope. Resilience is assessed as 'Very low' as the Magallana gigas population would need to be removed for recovery to occur. Hence, sensitivity is assessed as 'Medium'. The confidence in the assessment is 'Low' because the sensitivity of this biotope to Magallana gigas is potentially site-specific and there is a risk of its introduction by artificial means. 

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

A recent review of parasites, pathogens and commensals identified a range of agents impacting European cockles, including 50 conditions affecting Cerastoderma edule (Longshaw & Malham, 2013). Cockles are hosts to viruses, bacteria, fungi, Apicomplexa , Amoeba, Ciliophora, Perkinsozoa, Haplosporidia, Cercozoa, Turbellaria, Digenea, Nematoda, Crustacea and Nemertea.  Mortalities are associated particularly with digeneans and some protistan infections; parasites may limit growth, reduce fecundity and alter burrowing behaviour (Longshaw & Malham, 2013). A number of examples of conditions associated with mass mortalities of Cerastoderma edule are presented below.  Parasites and disease are more likely to cause mortalities in populations that are subject to suboptimal conditions or other stressors such as hot summers or cold winters (Longshaw & Malham, 2013).  Experimental infection of Cerastoderma edule with a trematode parasite showed that effects differed depending on habitat conditions (Wegeberg & Jensen, 2003). Infected Cerastoderma edule reared in sub-optimal conditions lost more body weight than infected cockles in more optimal habitats and did not regain condition when placed in higher shore habitats where immersion and food supply was limited.  Infected cockles placed on lower shore sites with longer emersion times regained condition despite the infection and were equivalent to controls. The impact of trematodes is therefore mediated by habitat conditions and in some instances may have no effect (Wegeberg & Jensen, 2003).

Infestation by a trematode parasite Cercaria cerastodermae impairs the burrowing ability of Cerastoderma edule and was identified as the likely cause of a mass mortality of cockles in Scandinavian waters in 1991 (Jonsson & André, 1992). Another trematode parasite Gymnophallis choledochus may castrate Cerastoderma edule, reducing reproduction and recruitment and indirectly leading to population declines (Thieltges, 2006).

An unidentified amoeba, measuring 18–20 mm in diameter, was described from the sub-epithelial gill tissues of Cerastoderma edule from Portugal (Azevedo, 1997). The amoeba was associated with haemocytic infiltration and necrosis of host cells. Affected cockles were found gaping at the surface and the infection was considered to be responsible for mass mortalities.

Cockles also suffer from disseminated neoplasia-a leukaemia like disease associated with mass mortalities. Cerastoderma edule from Ireland have been reported to be especially susceptible (Barber et al., 2004). High mortalities of cockles observed in north west Spain in 1997 were associated with a higher prevalence (up to 84%) of disseminated neoplasia compared to control areas (4% prevalence) not experiencing mortality (Villalba et al. 2001).

Sensitivity assessment. The available evidence suggests that Cerastoderma edule is susceptible to a range of pathogens and parasites. The effects of these may be exacerbated by stressors such as short immersion times and thermal stress (amongst others). As evidence exists for mass mortalities, resistance is assessed as ‘Low’ and resilience is assessed as ‘Medium’. Sensitivity is therefore categorised as ‘Medium’.

Removal of target species

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

Evidence

The sedimentary biotope and characterizing and associated species may be disturbed and damaged by static or mobile gears that are targeting Cerastoderma edule or other species. These direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures. The sensitivity assessment for this pressure considers any biological/ecological effects resulting from the removal of target species on this biotope. Dense populations of Cerastoderma edule on intertidal flats support commercial fisheries in several areas of the UK and the species is also harvested throughout Europe. Harvesting may use mechanical methods (e.g. tractor dredges or hydraulic suction dredging) or hand collection using rakes or other methods. The fishery is managed through local bylaws and local target size classes are set (usually cockles below 20 mm are not collected). The commercial importance of the fishery has stimulated research on impacts on cockles and the sedimentary habitat and associated species. In some habitats removal of Arenicola marina and Hediste diversicolor for fishing bait may occur but these species are not considered to characterize this biotope and the removal of these as target species is not considered in this review; the relevant biotopes (LS.LSa.MuSa.LimAre; SS.SMu.IFiMu.Are; LS.LMu.MEst.HedMac), characterized by these species contain more information. The physical effects of harvesting on this species are addressed in the physical disturbance sections. Removal of Cerastoderma edule (cockles) by targeted harvesting may result in an altered community and may alter the character and reduce the spatial extent of the Cerastoderma edule and polychaetes in the littoral muddy sand biotope.

Coffen-Smout (1998) studied simulated fisheries impacts on Cerastoderma edule and reported that the cockle shell withstood between 12.9 and 171.4 newtons (N) of force depending on shell size and position of load (a 1 kg weight exerts about 10 N). Cockles are often damaged during mechanical harvesting, e.g. 5-15% were damaged by tractor dredging (Cotter et al., 1997) and ca 20% were too damaged to be processed after hydraulic dredging (Pickett, 1973). Cook (1991) reported overall damage rates of 11-14% of rejects from rotary riddles on three hydraulic section dredgers operating. Undersized and rejected cockles may be stunned where these suffer prolonged vibrations from passage through mechanical gear and sorters, this can delay reburrowing, leading to increased predation and/or distribution by tidal waves and currents (Coffen-Smout & Rees, 1998).

Following size sorting (either mechanically or by hand), undersized cockles are deposited on the sediment surface. Damage rates and survival rates of harvested and discarded cockles and rates of reburrowing and displacement have been examined in a number of studies.   The sediment on which discards are deposited affects burrowing. Experimental displacement to stimulate harvesting impacts found that cockles deposited in pools are more able to rebury while none of those deposited on drained (and hence hard) sands were able to reburrow (Coffen-Smout & Rees, 1999). In this subtidal biotope, reburial rates should be high. Greater proportions of smaller cockles than medium or large reburrow, so that larger cockles are more likely to be displaced by tides (Coffen-Smnout & Rees, 1999). Cockles that were transported up to 200m on the flood tide could reburrow if habitats in the new position were suitable (Coffen-Smout & Rees, 1999).

The method of harvesting cockles will influence the proportions that are removed and damaged. Pickett (1973) found that intense dredging for a short period on a bed of cockle spat had little effect on survival and growth although Cook (1991) found that impacts on small cockles from dredging were variable, with little reduction one year but a reduction in density observed the following year. Cotter et al. (1997) assessed the catch rates and damage and mortality of Cerastoderma edule resulting from experimental tractor dredging at the Burry Inlet (Wales). Stocks of adult cockles were reduced by 31 and 49% in low and high density areas respectively. Similarly mechanical cockle harvesting in muddy sand reduced the abundance of Cerastoderma edule by ca 34%. Populations had not recovered their original abundance after 174 days (Ferns et al., 2000).

Hand raking for cockles on intertidal silty sandflats, using rakes that penetrated the surface by 5-10cm, resulted in a three-fold increase in the damage rate of cockles compared to control plots and, in the short-term, led to a relative decrease in the overall abundance of fauna (Kaiser et al., 2001). After 56 days the small (9m²) plots had recovered but the larger (36m²) plots remained in an altered state. Results collected over a year after the disturbance suggested that while effects of hand-raking may be significant within a year, they are unlikely to persist beyond this time-scale unless there are larger long-lived species present within the community (Kaiser et al. 2001).

The presence of dense cockle beds inhibit the establishment of other benthic species through space and resource competition, disturbance (Flach, 1996) and consumption of larvae (Andre et al., 2003). Removal of adult cockles by harvesting or other factors allows other species to establish. Following experimental removal of large adult Cerastoderma edule by Frid & Casear (2012) sediments showed increased biodiversity and assemblages dominated by traits common to opportunist taxa at a species-poor shore at Warton Sands, Morecambe Bay, and a more diverse shore at Thurstaston, Dee estuary. The movements of cockles disturb and exclude the amphipod Corophium volutator and other species (Flach, 1996; Flach & de Bruin, 1994) the removal of cockles may, therefore, allow this species to colonize intertidal flats. During periods of low cockle density, Desprez et al., (1992) observed that Pygospio elegans established dense populations; when cockles returned these were lost within one year.

It should be noted that removal of Cerastoderma edule by targeted harvesting may lead to wider ecological effects through starvation of shore birds in winter. This has been observed in the Dutch Wadden Sea (Smit et al., 1998). This effect is not directly of significance to this biotope and is not considered within the assessment.

Sensitivity assessment. Removal of the key characterizing species Cerastoderma edule by targeted harvesting would alter the character of the biotope and result in reclassification. The abundance of other soft-sediment infauna (particularly opportunist species such as Pygospio elegans and Capitella capitata may increase in disturbed patches in the short-term as a result of the removal of cockles resulting in reduced competition for space and predation (on larvae). Where sediments remain suitable cockles are likely to recolonize via adult migration, survival of small, discarded cockles or via larval recruitment.  In general fishing practices will be efficient at removing this species, resistance is therefore assessed as ‘Low’ (removal is not considered to be total as smaller individuals are not retained and harvesting is unlikely to be 100% efficient at removing larger cockles). Resilience is assessed as ‘Medium’ so that sensitivity is assessed as ‘Medium’. Recovery will be influenced by a range of factors as outlined in the resilience section. Small patches are likely to be in-filled by adult cockle movement, large patches will recover through larval recruitment, which again is subject to many factors, and may be improved by the removal of adult cockles. However, as Cerastoderma edule recruitment is episodic, a recovery of ‘Medium’ to represent the recovery of age-classes from broad-scale removal was considered appropriate. Biotope sensitivity is therefore assessed as ‘Medium’. Although some experiments have shown rapid recovery, the plots used in experiments are small and subject to low levels of harvesting compared to intertidal flats that are harvested at larger scales and where patches may be re-worked over a season.

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

Dense beds of Cerastoderma edule occur in situations where the faunal assemblage is species- diverse and productive, but also where very few taxa are present (Cesar, 2012). These observations suggest that Cerastoderma edule populations are not dependent on other species and are therefore unlikely to be impacted by ecological/biological effects from the removal of others species.  The removal of predators such as shrimp and crab may enhance recruitment of larvae (Beukema & Dekker, 2005). The physical effects of removal of other species such as polychaete worms targeted by bait diggers may, however, impact Cerastoderma edule and other species associated with this biotope, through direct damage and removal and displacement. These direct effects of sediment disturbance are assessed in the physical damage sections.

The removal of Cerastoderma edule and other associated species would alter the biotope from the description and change community structure (diversity, biomass and abundance), potentially altering ecosystem function and the delivery of ecosystem goods and services (including the supply of food to fish and birds).

Sensitivity assessment. The assessment considers whether the removal of characterizing and associated species as by-catch would impact the biotope. Lethal damage to and removal of Cerastoderma edule and other species as by-catch would alter the character of the biotope. As Cerastoderma edule and Macoma balthica and other species are either sedentary or incapable of rapid evasive movements, resistance is assessed as ‘Low’. Resilience is assessed as ‘Medium’ based on Cerastoderma edule and Macoma balthica and sensitivity is therefore categorized as ‘Medium’.  Physical damage to the sediment and other physical damage factors are considered in the abrasion and extraction pressures.