The Marine Life Information Network

Temperature increase (local)

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

Evidence

The important characterizing species Arenicola marina and Macoma balthica are adapted to living within the intertidal zone. Some resistance to temperature fluctuations is achieved by burying within the sediment, which buffers against acute temperature changes over the tidal cycle.

Sommer et al. (1997) examined sub-lethal effects of temperature in Arenicola marina and suggested a critical upper and lower temperature of 20°C and 5°C respectively in North Sea specimens. Above or below these critical temperatures specimens resort to anaerobic respiration. Sommer et al. (1997) noted that specimens could not acclimate to a 4°C increase above the critical temperature. Therefore, Arenicola marina is probably intolerant of a short-term acute change in temperature of 5°C although it is unlikely to be directly affected due to its infaunal habit. However, temperature change may adversely affect reproduction, for example, spawning can be inhibited in gravid adults maintained above 15°C and temperature change may affect maturation, spawning time, synchronization of spawning and reproduction in the long-term (Bentley & Pacey, 1992; Watson et al., 2000). Therefore, temperature change may affect lugworm recruitment in the long-term.

Arenicola marina's optimum temperature range appears region specific, with the optimum temperature range increasing as latitude decreases (Schroeer et al., 2009). Therefore, Arenicola marina in UK and Irish populations will occupy an optimum temperature range in relation to UK and Irish latitudes. An upper limit above 20°C may occur in more southerly populations.

In studies in Whitley Bay, Tyne and Wear, UK, Arenicola marina were most active in spring and summer months, with mean rate of cast production fastest in spring and particularly slow in autumn and winter, suggesting feeding rate is greatest in higher temperatures (Retraubun et al., 1996). Retraubun et al. (1996) also show that cast production by specimens in lab experiments increased with temperature, peaking at 20°C before declining. Rates of cast production at 30°C were still higher than at 10°C, suggesting UK populations may have greater tolerance to higher temperatures than populations studied in more northerly latitudes. Tolerance to temperature changes within specific regions, such as a 5°C increase for one month or a 2°C for one year would be relative to the existing temperature in that region and intolerance of an acute temperature change of 5°C is still probable.

Temperature change may affect maturation, spawning time and synchronisation of spawning and reproduction in the long-term (Watson et al., 2000). However, spawning success would remain dependent upon spring and autumn temperatures the seasons when spawning occurs in relation to spring and neap tides, remaining below 13-15°C. Additionally, impact from temperature change at the substratum surface may be mitigated as, being a burrowing species, Arenicola marina are protected from direct effects. Increased temperatures may affect infauna indirectly, by stimulating increased bacterial activity, increased oxygen consumption and therefore depletion of oxygen from the interstitial waters resulting in reduced oxygen levels (hypoxia) or absence of oxygen (anoxia) in the sediment (Hayward, 1994). De Wilde & Berghuis (1979) reported 20% mortality of juveniles reared at 5°C, negligible mortality at 10 and 15°C but 50% mortality at 20°C and 90% at 25°C. Schroeer et al. (2009) identified a shift in the thermal window of Arenicola marina, with an optimum towards higher temperatures with decreasing latitudes, suggesting the species may adapt to long-term shifts such as a 2°C but over a time period beyond the one-year benchmark pressure.

In Europe, Macoma balthica 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. However, Barda et al. (2014) found that increased temperature reduced growth rates in populations in the Baltic Sea. Beukema et al. (2014) also warn that increasing water temperatures as a result of global warming are likely to shorten the growing season (typically late winter to early spring) if warmer spring and summer water temperatures are experienced. Jansen et al. (2007) suggest that temperature increases on the Spanish coast along the Bay of Biscay over the past 40 years have caused loss of Macoma balthica populations, due to short-term but frequent exposure to >30°C in the Spanish estuaries, which induced elevated maintenance rates in Macoma balthica, and ultimately starvation. Jansen et al. (2007) predict the southern limit of the species will progressively shift north if temperatures continue to rise. It seems likely, therefore, that the Macoma balthica could tolerate a chronic change in UK waters with limited mortality but the length of the growing season will likely be reduced if a short-term 5°C temperature increase in temperature for one month period occurred during winter or spring months, or a long-term increase of 2°C for one year.

Both of the polychaete species that are typically superabundant and common in the biotope, Scoloplos armiger and Pygospio elegans, show a relationship between timing of reproduction and temperature. Studies on the polychaete Scoloplos armiger in the Wadden Sea (North Sea) displayed that intertidal ‘Type I’ Scoloplos armiger reproduce in spring, through holobenthic development, triggered by a rise in seawater temperature above 5°C (Kruse et al., 2004). Gibson & Harvey (2000), in a study on asexual reproduction of Pygospio elegans in Nova Scotia, Canada, found temperature did not influence reproduction strategy (planktotrophy, lecithotrophy or asexual reproduction) but that environmental conditions, including temperature, influence timing of reproduction. Anger (1984) found a population in the Kiel Bight, Baltic Sea to also reproduce exclusively through asexual reproduction while two additional populations were predominantly sexual (Anger, 1984).

Both Scoloplos armiger and Pygospio elegans tolerate a wide temperature range although optimal temperature ranges, based on feeding and reproductive success are more restricted, suggesting a 5°C increase in temperature over a month may increase temperatures above the preferred range, but not cause widespread mortality. Pygospio elegans has been recorded in seas with a temperature range of 1.6°C to 12.5°C (OBIS, 2016). Scoloplos armiger occurs in seas with a temperature range of between 8.8°C and 13°C (OBIS, 2016). These temperature ranges are not derived from peer reviewed studies and therefore caution should be used with the interpretation.

Sensitivity assessment.  Therefore, of the species characterizing the biotope, Arenicola marina would be least tolerant of a 5°C increase in temp for one month period, or 2°C for one year. Other species characterizing the biotope may tolerate this pressure at the benchmark levels but timing of reproduction may be impacted. Impacts on timing of reproduction may affect recruitment in the long-term.

A resistance of ‘Medium’ has been assigned. In general, impacts to reproduction of species characterizing the biotope would rate as high resistance, however, for the biotope resistance was raised to medium as Arenicola marina specimens were shown not to acclimatise to a 4°C rise above 20°C (Sommer et al., 1997; Sommer & Portner, 1999). A 5°C increase in temperature for a one month period may also extend periods during the year when temperatures exceed the preferred range of the polychaete species Scoloplos armiger and Pygospio elegans, dependent on the season the change occurred in (e.g. occurring in winter, spring and autumn).

Based on lifespan and age at sexual maturity, Arenicola marina (5-6 years lifespan, maturity reached at 1-2 years) recovery of populations may take over 2 years suggesting resilience is ‘Medium’ (2-10 years) for this characterizing species. Additional pressures such as presence of suitable sediments will also affect recovery times (Marine Ecological Surveys Limited (MES), 2008).

Resistance to an acute and chronic change in temperature at the pressure benchmark is assessed as ‘Medium’ and recovery as ‘High’ and the biotope sensitivity is considered ‘Low’ at the benchmark level. The timing, strength (°C change) and duration will also affect recovery times. For instance timing of acute changes may lead to greater impacts, temperature increases in the warmest months may exceed thermal tolerances whilst changes in colder periods may stress individuals acclimated to the lower temperatures. Local populations may be acclimated to the prevailing temperature regime and may, therefore, exhibit different tolerances to populations from other latitudes. Therefore, caution should be used when inferring tolerances from populations in different regions.

Temperature decrease (local)

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

Evidence

Arenicola marina displays a greater tolerance to decreases in temperature than to increases, although optimum temperatures are reported to be between 5°C and 20°C. Sommer et al. (1997) report populations in the White Sea (sub polar) acclimatised to -2°C in winter. Populations in the North Sea (boreal) were less tolerant of temperatures below 5°C, although in laboratory experiments on individual lugworms from North Sea populations worms survived a temperature drop from 6 or 12°C to -1.7°C for more than a week (Sommer & Portner, 1999).

Spawning success is dependent upon spring and autumn temperatures, the seasons when spawning occurs in relation to spring and neap tides, remaining below 13-15°C. Temperature change may affect maturation, spawning time and synchronization of spawning and reproduction in the long-term (Watson et al., 2000). De Wilde & Berghuis (1979) reported 20% mortality of juveniles reared at 5°C, negligible mortality at 10°C and 15°C but 50% at 20°C and 90% mortality at 25°C (Tyler-Walters, 2008).

Temperature change at the pressure benchmark levels may impact timing of reproduction. The preferred spring and autumn temperature for spawning to occur and juvenile mortality to be negligible (13-15°C) may be extended into late spring and early autumn months. There is, however, increased risk in winter and early spring months of juvenile mortality at low temperatures (at or below 5°C), in particular if the pressure benchmark of a 5°C decrease in temperature for one month occurs during these periods.

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 in seas around the UK and Ireland Macoma balthica would be intolerant of decreases in temperature at the benchmark level.

Both of the polychaete species that are typically superabundant and common in the biotope, Scoloplos armiger and Pygospio elegans, show a relationship between timing of reproduction and temperature. Studies on the polychaete Scoloplos armiger in the Wadden Sea (North Sea) displayed that intertidal ‘Type I’ Scoloplos armiger reproduce in spring, through holobenthic development triggered by a rise in seawater temperature above 5°C (Kruse et al., 2004). Timing of reproduction of Pygospio elegans in a study from the Baltic Sea was linked to environmental conditions including temperature (Anger, 1984). A 5°C decrease in temperature for a one month period, or a 2°C decrease for one year would remain within the preferred temperature range Pygospio elegans occurs within (1.6 °C to 12.5 °C) (OBIS, 2016). However, these benchmark temperature decreases would potentially result in winter temperatures below the optimum range for Scoloplos armiger (of between 8.8°C and 13°C) but remain within the range the species occurs within (-2.1°C and 29.5°C) (OBIS, 2016).

Sensitivity assessment.  Species characterizing the biotope may resist this pressure at the benchmark levels but timing of reproduction may be impacted. Impacts on timing of reproduction may affect recruitment in the long-term. Due to the natural range and resistance of low temperatures of Arenicola marina, Macoma balthica and both the typically superabundant and common polychaete species in the biotope, Scoloplos armiger and Pygospio elegans it is unlikely that a change in the pressure at the benchmark will have a significant impact on condition of this biotope. Therefore, this biotope is assessed to have 'High' resistance to decreased temperatures at the benchmark (acute and chronic). Therefore, resilience is 'High' and this biotope is assessed as 'Not Sensitive' at the benchmark level.

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 recorded from variable to fully marine (Connor et al., 2004). An increase of one MNCR salinity category would be to fully marine 30-40 ‰ or beyond this level to >40‰. Arenicola marina would be expected to exhibit reduced tolerance to an increase in salinity as the species reached highest densities in estuarine systems in Welsh study sites (Cadman, 1997). However, Arenicola marina exposed to hyper-osmotic shock (47 psu), lose weight, but are able to regulate and gain weight within 7-10 days (Zebe & Schiedek, 1996).

Environmental fluctuations in salinity are only likely to affect the surface of the sediment, and not deeper buried organisms, since the interstitial or burrow water is less affected. However, under longer term or permanent increase in salinity, sediment waters would be expected to also adjust. Behavioural responses are shown by Arenicola marina to cope with rapid salinity changes in the intertidal. The animals withdraw in their burrows when the salinity is unfavourable, and remain inactive except for infrequent "samplings" of the overlying water (Spaargaren & Weber, 1979).

Macoma balthica is found in brackish and fully saline waters but is more common in brackish waters (Clay, 1967b) so may tolerate a state of flux. Seitz (2011) found Macoma balthica (as Macoma balthica) distribution across a salinity gradient between a minimum and maximum of 8.8 psu to 19 psu in Cheaspeake Bay was not influenced by salinity. Instead, resource availability was the principal influence on Macoma balthica at a broad scale, suggesting changes in one MNCR salinity category would have limited impact. McLusky & Allan (1976) reported that Macoma balthica (as Macoma balthica) failed to grow at 41 psu. It is likely that Macoma balthica would be tolerant of an increase in salinity category to fully marine but further increases to >40 ‰ are likely to affect growth and condition.

In the western Baltic Sea Scoloplos armiger abundance was greatest between 12 psu and 17 psu and reduced abundance with increasing salinity was observed (Gogina et al., 2010). As Scoloplos armiger is a species complex and is not a cosmopolitan species there may be inconsistencies between general environmental setting found in literature and observed and predicted distribution limits within study sites (Bleidorn et al., 2006 cited in Gogina et al., 2010). Pygospio elegans is common in both marine and brackish waters in the Schelde estuary (Netherlands) suggesting in European habitats the species tolerates a broad salinity range (Ysebaert et al., 1993). Studies of Pygospio elegans population structure in the Baltic Sea and North Sea also found larvae were not hampered by changes in salinity (Kesaniemi et al., 2012). Although case studies are lacking for British and Irish coasts, the existing evidence suggests Pygospio elegans would tolerate salinity changes at the pressure benchmark level.

Although increases in salinity are tolerated by these polychaete species an increase in one MNCR salinity category above the usual range of the biotope may reduce abundance as both species are most abundant in variable and fully marine salinity categories (and Scoloplos armiger has displayed negative responses to increasing salinity).

Sensitivity assessment.  A short-term increase in one MNCR salinity category above the usual range of the biotope/habitat is likely to negatively impact body condition and growth of characterizing species of the biotope. Hypersaline conditions are likely to cause mortality to characterizing species. For extended periods this will impact the biotope but if salinity conditions return to those characterizing the biotope recovery is likely in 1-2 years and full recovery of populations in 2-10 years. Resistance to changes at pressure benchmark level is ‘Medium’. Arenicola marina and Macoma balthica both have lifespans of 5-10 years and generation times of 1-2 years, resilience (recovery) would be expected in 1-2 years, following restoration of salinity regime, therefore giving a ‘High’ resilience and a sensitivity of ‘Low’. 

Salinity decrease (local)

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

Evidence

Arenicola marina is unable to tolerate salinities below 18-24 psu and is excluded from areas influenced by freshwater runoff or input (e.g. the head end of estuaries) where it is replaced by Hediste diversicolor (Barnes, 1994; Hayward, 1994). Once the salinity of the overlying water drops below about 55% seawater (about 18 psu) Arenicola marina stops irrigation, and compresses itself at the bottom of its burrow. It raises its tails to the head of the burrow to 'test' the water at intervals, about once an hour. Once normal salinities return they resume usual activity (Shumway & Davenport, 1977; Rankin & Davenport, 1981; Zebe & Schiedek, 1996). This behaviour, together with their burrow habitat, enabled the lugworm to maintain its coelomic fluid and tissue constituents at a constant level, whereas individuals exposed to fluctuating salinities outside their burrow did not (Shumway & Davenport, 1977). Environmental fluctuations in salinity are only likely to affect the surface of the sediment, and not deeper organisms, since the interstital or burrow water is little affected. However, lugworms may be affected by low salinities at low tide after heavy rains. Arenicola marina was able to osmoregulate intracellular and extracellular volume within 72-114 hrs by increased urine production and increased amino acid concentration in response to hypo-osmotic shock (low salinity) (see Zebe & Schiedek, 1996).

Arenicola marina in the Baltic are more tolerant of reduced salinity. For example, Barnes (1994) reports that Arenicola marina occurs at salinities down to 18 psu in Britain, but survives as low as 8 psu in the Baltic, whereas Shumway & Davenport (1977) reported that this species cannot survive less than 10 psu in the Baltic. The reported salinity tolerance in the Baltic is probably a local adaptation.

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, 1967b) 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. Metabolic function should, however, return quickly to normal when salinity returns to original levels. Decreased salinity may also affect the ability of Macoma balthica to tolerate contaminants such as heavy metals (see Bryant et al., 1985, 1985a). Usually, contaminants become more toxic at low salinity (Langston, W.J. pers comm.).

Scoloplos armiger shows a lower salinity limit of 10.5 psu (Gogina et al., 2010), suggesting the species is tolerant of a decrease from the variable salinity category to the reduced salinity category and even the low salinity category in the MNCR scale. Pygospio elegans was common in both marine and brackish waters in the Schelde estuary (Netherlands) suggesting in European habitats the species tolerates a broad salinity range (Ysebaert et al., 1993). Studies of Pygospio elegans population structure in the Baltic Sea and North Sea also found larvae were not hampered by changes in salinity (Kesaniemi et al., 2012). Although case studies are lacking for British and Irish coasts the existing evidence suggests Pygospio elegans would tolerate salinity changes at the pressure benchmark level.

Sensitivity assessment. The characterizing species within the biotope occupy between ‘variable’ and ‘fully marine’ category salinities and can tolerate greater osmotic stress for short periods, caused by decreases in salinity below 18 ?⁄?? (the lower limit for ‘low’ category salinity). Resistance to the assessed decrease in salinity from variable (18-35 ?⁄??) to reduced (18-30 ?⁄??) is probably ‘High’, so that resilience is also ‘High’ and the biotope is assessed as ‘Not Sensitive’ at the benchmark level.

Freshwater run-off may cause a further decrease, beyond just one salinity category, to the ‘low’ salinity category. Abundance of key characterizing species may be limited or growth rates reduced from the long-term exposure to reduced salinity. The biotope would be replaced by those dominated by species occurring in lower salinities such as Hediste diversicolor. Resistance following long-term exposure to the ‘Low’ category (below 18 ?⁄??) would be ‘medium’ and recovery ‘Medium’. Sensitivity under this further decrease in salinity would, therefore, be ‘Medium’ (if a decrease continued beyond one salinity category).

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

A local change in water flow is likely to have a greater impact on sediment transport than direct impacts on populations of Arenicola marina. At low current velocities Arenicola marina casts and burrows enable the deposition and adherence of macroalgae (Puls et al., 2012).  At high current velocities Arenicola marina faecal casts are quickly eroded and sediment particles are suspended in the water column. As suspended particles (in particular fine particles) may be transported away by water currents, this process, over time, can facilitate a gradual change of sediment properties in the entire bioturbated sediment layer (to the depth of worm burrows). Therefore, an increase in water flow may cause the depletion of fine particle matter, leaving coarser particles and change the sediment type (Wendelboe et al., 2013). Coarser sediment may influence populations of other species within the biotope, such as Macoma balthica which prefers finer particle sizes and Scoloplos armiger and Pygospio elegans that thrive in medium particle sizes.

Macoma balthica is likely to experience greater impact from increased water flow as the species thrives in low energy environments, such as estuaries that characterize the biotope (Tebble, 1976). Macoma balthica also shows preference for substratum that has a high proportion of fine sediment (Budd & Rayment, 2001). Increased water flow rate is likely to change the sediment characteristics in this biotope, primarily by re-suspending and preventing deposition of finer particles (Hiscock, 1983). This would result in erosion of the preferred habitat, which may cause mortality of some portion of the population of Macoma balthica. Higher current velocity (0.18 m/s ) recorded in flume experiments conducted in the Isle of Sylt (North Sea) led to juvenile Macoma balthica being washed out of the sediment (Zuhlke & Reise, 1994). 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.

Sensitivity assessment. A decrease in water flow may result in accretion of fine sand, and, thereby, a change to muddy sand and mud. As the biotope occurs in association with muddy sand or fine sand a decrease in water flow is unlikely to impact the biotope (although under an excessive deposition of mud or silt, mud communities, e.g. HedLim, may replace the biotope, but this is unlikely at the benchmark levels).

Finer sediment has a predicted threshold velocity (flow velocity at which fine grain size sediment would be picked up from the sea bed) of ~0.05 m/s (Gray & Elliott, 2009), therefore an increase of 0.1-0.2 m/s may cause a significant change in grain size of sediments. Although resistance is ‘None’ if cases occurred where Macoma balthica was replaced by another tellin species as the biotope would be altered, and resilience is probably ‘Medium’. The resulting sensitivity score is ‘Medium’ given the potential scenario that an increase in peak mean spring bed flow velocity of between 0.1 m/s to 0.2 m/s for more than 1 year may result in a characterizing species, Macoma balthica being replaced by another species. 

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

When the burrow of the lugworm Arenicola marina is emersed, ventilation becomes impossible and the animal is exposed to increasing hypoxia (see de-oxygenation section below). Partial pressure of dissolved oxygen (pO?) in the remaining water of the lugworm burrow has been shown to decrease from 33 to 13 torr during 2 hours of tidal emersion (Jones, 1955 cited in Volkel et al., 1995). During periods when burrows are not covered (by seawater), blood oxygen drops close to 0 within 1 hour of emersion (Toulmond, 1973), Arenicola marina reduces its ventilation movements and O? consumption and switches from aerobic to anaerobic metabolism (Schottler et al., 1984; Toulmond & Tchernigovtzeff, 1984; Toulmond, 1987). When the tide comes back in, Arenicola marina returns to aerobic metabolism and tissue metabolites return to pre-emersion levels within 1 to 2 hours (Portner et al., 1979).

An increase in time not covered by the sea for a period of ≥1 year or a decrease in high water level for ≥1 year will increase the time Arenicola marina spends metabolising anerobically. This is likely to reduce abundance, as survivability of Arenicola marina during spawning times has been shown to be reduced dramatically during anaerobic conditions (Schottler, 1989). Coosen et al. (1994) found that in an intertidal estuary in the south-west Netherlands settlement of juvenile Arenicola marina was interrupted during periods of reduced tidal amplitude. Therefore, adult and juvenile populations are likely to be negatively impacted under this pressure at the benchmark level. Increased emergence, however, will increase the risk of hypoxia and anoxia (see de-oxygenation). Increased emersion is likely to result in a depressed upper limit of the species on the shore, especially in juveniles.

An increase in relative sea level has been related to an increase in Arenicola marina abundance in the upper tidal zone in eastern North Sea mudflats since the 1930s (Reise et al., 2008). Arenicola marina typically occupy the higher intertidal shore, exposed even on neap low tides, and the black lug Arenicola defodiens is dominant in communities further down the shore, in regions only exposed at spring low water. A change in relative sea level or time covered by seawater is likely to result in changes in spatial distribution of the species. Decreased emergence is likely to increase the extent of the Arenicola marina population higher on the shore (but lower on the shore the upper extent of Arenicola defodiens may increase).

Macoma balthica occurs in the upper regions of the intertidal (Tebble, 1976) and is therefore likely to be tolerant of prolonged emergence. It is a bivalve and can close tightly by contraction of the adductor muscle, storing moisture inside the shell. The silty sediments in which the species lives have a high water content and are therefore resistant to desiccation. Furthermore, Macoma balthica is mobile and able to relocate in the intertidal by burrowing (Bonsdorff, 1984) or floating (Sörlin, 1988). It would be expected to react to an increase in emergence by migrating down the shore to its preferred position. There may be an energetic cost to this migration but it is not expected that mortality would result. Macoma balthica should quickly recover from the energetic cost of relocation.

Macoma balthica occurs in the intertidal and sublittorally down to depths of 190 m (Olafsson, 1986), although is more abundant in the intertidal, so would be expected to be tolerant of a decrease in emergence regime. However, a case study predicting changes in biomass of Macoma balthica in the Humber Estuary, UK (western North Sea) under expected sea level rise conditions displayed negative impacts. As the coastal squeeze resulting from sea level rise would produce steeper and more homogenous beach face profiles, biomass of Macoma balthica was predicted to decrease (Fujii & Raffaelli, 2008). The sensitivity assessment given in relation to the benchmark pressure should, therefore, be interpreted in relation to intertidal habitat availability following the relative sea level changes.  

Scoloplos armiger occurs from <1 to 113 meters depth (OBIS, 2016). Two sympatric sibling species have been suggested for  Scoloplos armiger, ‘Type I’ living in the intertidal zone and ‘Type S’ living subtidally (Kruse et al., 2004). Schueckel et al. (2013) show depth was a significant variable influencing Scoloplos armiger abundance in intertidal zones within Jade Bay (Wadden Sea). Scoloplos armiger occurred in greatest abundance in the two intertidal communities associated with longest submergence times (14 hours and 24 hours saturated) (Schueckel et al., 2013). A change in relative sea level and change in time covered may influence abundance. A decrease in time covered, would likely reduce the upper limit of the biotope on the shore (as the Scoloplos armiger population would be redistributed to lower down the shore). An increase in time covered or an increase in relative sea level may result in Scoloplos armiger becoming constantly subtidal. Under a decrease in emergence 'Type I’ Scoloplos armiger populations are likely to be replaced by 'Type S’ Scoloplos armiger populations. This change is based upon findings of Kruse & Reise (2003) that, for North Sea Scoloplos armiger populations, genetically distinct 'Type I’ and 'Type S’ populations occur. Instead of settling across intertidal and subtidal habitats, juveniles hatched from cocoons (Type I) in the intertidal suffer high mortality when translocated from the intertidal. Meanwhile, pelagic larvae of subtidal origin (Type II) either find their way back to subtidal habitat or suffer high post-settlement mortality in the intertidal (Kruse & Reise, 2003).

Sensitivity assessment. Emergence regime changes are likely to alter the upper and lower extent of the biotope.  Although species characterizing the biotope may tolerate increased emersion, a decrease in high water level, increasing the time the biotope is not covered by the sea ≥ 1 year, is likely to reduce survivability and abundance.

All species characterizing the biotope may be resistant to decreased emergence and this is likely to increase the extent of the characterizing species Arenicola marina higher on the shore, however, lower portions of the biotope may be colonized by Arenicola defodiens. Populations of the superabundant polychaete Scoloplos armiger ('Type I’) would increase in the upper shore but in the lower shore 'Type S’ Scoloplos armiger (that occupy subtidal habitats) would dominate. The upper and lower extent of the biotope are likely to move further up the shore.

As a combined assessment, taking account of both benchmarks, Resistance in ‘Low’ due to the impact of increased emergence on survivability of Arenicola marina, especially during spawning times. Resilience is ‘Medium’ and sensitivity is ‘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

Evidence is limited for the effect of wave exposure changes on characterizing species and therefore the confidence in this assessment is low. Increased wave action results in increased water flow in the shallow subtidal. This is likely to have similar impacts to those under the pressure; ‘water flow changes’. A significant increase in water flow may result in a move to medium to coarse sand, a change that is likely to alter the biotope. However, this biotope occurs in moderate exposure to extreme shelter and at the benchmark level there is unlikely to be a significant change in sediment.  Wave mediated water flow tends to be oscillatory, i.e. moves back and forth (Hiscock, 1983), and may result in dislodgement or removal of individuals while covered at high water. As characterizing species live relatively deeply in the sediment this behaviour is likely to provide some tolerance to increases in wave exposure (Coosen et al., 1994).

Arenicola marina occupies moderately exposed through to very sheltered exposure and is therefore considered llikely to tolerate a change in nearshore significant wave height >3% but <5%.

To avoid the danger of being washed out of the substratum, wave action stimulates Macoma balthica to start burrowing and individuals have been shown to continue burrowing for a longer period of time than in still water (Breum, 1970). Limited zoobenthic biomass was recorded in areas exposed to strong currents and wave action (Beukema, 2002), however, impacts from this pressure at the benchmark level may be low for this biotope, as the biotope is limited to sheltered locations. Increases in wave action may therefore remain within the limits of the species tolerance but factors such as sediment redistribution may alter the physical biotope.

Sensitivity assessment. Resistance to a change in nearshore significant wave height >3% but <5% of the two main characterizing species Arenicola marina and Macoma balthica is ‘High’, given that the biotope occurs in very sheltered locations and an increase in nearshore significant wave height of >3% but <5% would continue to result in sheltered conditions which are within the species' tolerance limits. At the highest benchmark pressure (5% increase) the species exhibit resistance through their traits to live relatively deep in the sediment. Resilience (recoverability) is also ‘High’ giving a sensitivity of ‘Not Sensitive’. Due to limited evidence, confidence in this assessment is 'Low'.

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. Bryan (1984) reported that short-term toxicity in polychaetes was highest to Hg, Cu and Ag, declined with Al, Cr, Zn and Pb with Cd, Ni, Co and Se being the least toxic. It was recorded that polychaetes have a range of tolerances to heavy metals levels of Cu, Zn, As and Sn being in the order of 1500-3500 µg/g. 

Bat & Raffaelli (1998) reported 100% mortality of Arenicola marina exposed to the highest tested concentrations of copper, zinc, and cadmium 87, 101 and 76 μg/g, respectively. Campbell et al. (2014) investigated the effects of ocean acidification and copper toxicity on the early life stages of the polychaete Arenicola marina. Sperm motility was reduced by up to 4% by exposure to copper concentrations of 2 and 20 μM. And further reduced by 46% because of the combined stressors of copper and reduced pH. Exposure to copper or reduced seawater pH individually, reduced fertilization success significantly. Exposure to copper or reduced seawater pH individually had no significant effect on larval survival. However, there was a strong significant interaction under the combined stress of copper and reduced pH, with a 24% reduction in larval survival after five days of exposure. Casado-Martinez et al. (2008) reported a significant correlation between lugworm mortality and mercury concentration in sediments with up to 80% mortality but as the control sediment showed 15–20% mortality there was the potential that mortality could have been caused by other sediment conditions and not related to chemical stress. Rasmussen & Andersen (2000) reported that cadmium contamination increased the susceptibility of Arenicola marina to hypo-osmotic stress.  Overall, the evidence suggests that Arenicola marina can experience severe mortality due to exposure to copper, cadmium, mercury, and zinc. Therefore, its resistance to ‘transitional ‘metals’ is assessed as ‘None’, resilience as ‘Medium’, and sensitivity as ‘Medium’.

Arenicola marina was found to accumulate As, Cd, Sb, Cu, and Cr when exposed to pulverised fuel ash (PFA) in sediments (Jenner & Bowmer, 1990). Jenner & Bowmer (1990) also noted 95% mortality when exposed to 100% PFA for 90 days and 75% exposed to 50% PFA for the same period, however, the above mortality may have been due to the unsuitability of PFA as a substrate rather than the heavy metal contamination.

‘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. The remaining metals were reported to result in no mortality or sublethal effects. 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’.

‘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’.

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.

The evidence on the effects of tributyltin on Arenicola spp. was limited to two papers, one of which was not accessible (Walsh et al., 1984). Beaumont et al. (1989) reported that non-introduced Nereis diversicolor, Arenicola marina, and Eteone sp. occurred in the low-level TBT and the control treatments but not in the high-level TBT treatments. Overall, only sublethal effects were reported in the evidence reviewed. Therefore, the sensitivity of A. marina to TBT is assessed as ‘Not sensitive’ but with ‘Low’ confidence due to the lack of evidence. Similarly, the evidence for the effects of nanoparticulate metals, that is, nanoparticulate titanium was limited to a single study (Galloway et al., 2010). Only sublethal effects were reported in the evidence reviewed. Therefore, the sensitivity of A. marina to nanoparticulate titanium is assessed as ‘Not sensitive’ but with ‘Low’ confidence due to the lack of evidence.

Overall sensitivity assessment for this pressure. The worst-case resistance of the dominant characteristic species Arenicola marina and Macoma balthica to 'transitional metal and organometal' exposure is assessed as 'None' based on the evidence of the effects of 'transitional metals'.  Hence, resilience is assessed as ‘Medium’ and sensitivity as ‘Medium’. Where present Cerastoderma edule is also likely to be sensitive to transitional metal and organometal exposure. 

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. Suchanek (1993) concluded that, in general, in soft sediment habitats, infaunal polychaetes, bivalves and amphipods were particularly affected by oil spills. Hailey (1995) cited substantial kills of Nereis, Cerastoderma, Macoma, Arenicola and Hydrobia as a result of the Sivand oil spill in the Humber estuary in 1983. 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).  The Amoco Cadiz oil spill resulted in reductions in abundance, biomass, and production of the affected invertebrate communities. However, Nephtys hombergii and other polychaetes (cirratulids and capitellids) were largely unaffected by the Amoco Cadiz oil spill (Conan, 1982). The sediment rapidly recovered and in 1981, benthic recruitment occurred under normal conditions (Dauvin, 1998).

Hydrocarbons and PAHs, including dispersants.  Levell (1976) examined the effects of experimental spills of crude oil and oil-dispersant (BP1100X) mixtures on Arenicola marina. Single spills caused 25-50% reduction in abundance and an additional reduction in feeding activity. Up to four repeated spillages (over a 10-month period) resulted in complete eradication of the affected population either due to death or migration out of the sediment. Levell (1976) noted that recolonization was inhibited but not prevented. Prouse & Gordon (1976) examined the effects of surface fuel oil contamination and fuel oil sediment mixtures on the blow lug in the laboratory. They found that the blow lug was driven out of the sediment by a waterborne concentration of >1 mg/l or sediment concentration of >100 µg/g. Worms forced out of sediment may be able to migrate out of the affected area but will be exposed to severe predation risk, especially in daylight. Seawater oil concentrations of 0.7 mg oil/l reduced feeding after 5 hours and all worms exposed for 22 hours to 5 mg/l oil left the sediment and died after three days. However, the sample size in this experiment was very small (six worms). A sediment concentration >10 µg/g could reduce feeding activity. Arenicola marina can recolonize sediment relatively quickly (within one month), however, contaminated sediments would probably take longer to recover, extending recovery times.

Lewis et al. (2008) reported that both the WAF of crude oil and the PAH fluoranthene adversely affected fertilization success and caused larval mortality in Arenicola marina. Morales-Caselles et al. (2008) noted that sediment contaminated with fuel oil from a sunken tanker caused significant mortality in Arenicola marina, for example, 8% fuel oil/dry weight sediment resulted in 100% mortality after 21 days. Farke & Gunther (1984) and Morales-Caselles et al. (2009) demonstrated that oil-contaminated sediment reduced burrowing activity in Arenicola marina. Farke & Gunther (1984) noted that dispersed oil also reduced burrowing activity but the dispersant used showed no effect. The evidence suggests that oil contamination could also reduce recruitment to contaminated sediment, and hence prolong recovery. However, exposure of adult Arenicola marina to PAHs (Casado-Martinez et al., 2008) did not contribute to mortality.

Therefore, the resistance of Arenicola marina to petrochemical hydrocarbons is assessed as ‘None’ based on the worst-case results reviewed. Hence, resilience is ‘Medium’ and sensitivity is assessed as ‘Medium’. The evidence suggests that dispersed oils and dispersants only caused sublethal effects. Hence, its sensitivity to dispersed oils and dispersants is also assessed as ‘Medium’ but with ‘Low’ confidence due to the limited number of studies reviewed. The PAH flouranthene was reported to cause severe mortality in A. marina larvae, which may result in population decline in the long term. Therefore, the resistance of Arenicola marina to PAHs is assessed as ‘None’ based on the worst-case results reviewed but with ‘Low’ confidence. Hence, resilience is ‘Medium’ and sensitivity is assessed as ‘Medium’.

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). Therefore, the worst-case resistance of 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 for most of the papers reviewed. 

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). Macoma balthica was found in low numbers in the severely polluted area with a maximum abundance of species and the highest total biomass at 500 m from the discharge. Its abundance was greatest at 2.5-4 km from the discharge, while Eteone spp. and spionids were most abundant at 1-1.5 km (McLusky, 1982). However, the petrochemical discharge polluted the sediment within 500 m of the discharge but beyond that the effects were due to organic enrichment rather than the toxicity of petrochemicals alone (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. Therefore, 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.

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 of this pressure. The worst-case resistance of the dominant characteristic species Arenicola marina and Macoma balthica 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 for most of the papers reviewed. Where present, Cerastoderma edule is probably also of 'Medium' sensitivity. 

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. The effects of pesticides/biocides on Arenicola spp. were studied in six of the articles reviewed. Garnas et al. (1977) reported 100% mortality in Arenicola cristata exposed to 1000 µg/l Kepone for 5 days. Similarly, Rubenstein (1979) reported 100% mortality in Arenicola cristata exposed to 29.5 µg/l of Kepone, for 144 hours. Exposure to 2.8, 4.5, 6.6, 7.4, and 29.5 µg/l Kepone for 144 hours also reduced feeding behaviour significantly. However, Mirex and sodium pentachlorophenate reduced feeding and burrowing behaviour significantly (Schoor & Newman, 1976; Rubinstein, 1978) in Arenicola cristata. Carbaryl, Ivermectin and Parathion-ethyl were reported to cause significant mortality in Arenicola marina (Conti, 1987; Allen et al., 2007). Ivermectin had a significant effect on the survival of the lugworms; the 10-day LC50 was 17.9 µg IVM/kg wet sediment in Test 1 and 14.8 µg IVM/kg wet sediment in Test 2 and Ivermectin reduced the mean casting rate (Allen et al., 2007). Conti (1987) reported 48-hour LC50s of 2,700 µg/l for Parathion-ethyl and 7,200 µg/l for Carbaryl. Therefore, the worst-case resistance of Arenicola spp. to ‘Pesticides/biocides’ is assessed as ‘None’, resilience as ‘Medium’ and sensitivity assessed as ‘Medium’. The confidence is assessed as ‘low’ due to the limited evidence and the variation in toxicity between species and the chemicals tested.

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. Only two papers examined the effects of ‘Pharmaceuticals’ on Arenicola marina. Zanuri et al. (2017) investigated the impacts of Diclofenac, Ibuprofen, and Sildenafil citrate (Viagra®) on the fertilization biology of spawning marine invertebrates, including A. marina. Sperm motility and swimming speed were reduced when exposed to >1 µg/l Diclofenac for over 90 minutes. Ibuprofen exposure significantly increased the swimming speed of the sperm when exposed to >10 µg/l for 30 minutes or longer. Diclofenac negatively affected the fertilization success of the polychaetes but neither Ibuprofen nor Sildenafil citrate exposure affected fertilization success significantly. Pre-incubation of both sperm and oocytes caused significant decreases in fertilization success of the polychaetes at Diclofenac concentrations of 1 µg/l and above. Ibuprofen caused significant reductions in fertilization success when gametes were exposed to Ibuprofen at 1000 µg/l. Pre-incubation with Sildenafil citrate had no effects on fertilization success.  Lewis & Galloway (2009) reported that methyl methanesulfonate exposure did not affect fertilization success at all tested concentrations but abnormal development occurred at all tested concentrations (18, 32, and 52 mg/l for 24 hours and 72 hours prior to the induction of spawning) in polychaete Arenicola marina. Therefore, the sensitivity of Arenicola marina to ‘Pharmaceuticals’ is assessed as ‘Not sensitive’, but with ‘Low’ confidence due to the limited evidence. However, reported effects on larval development may have long-term effects on recruitment and population dynamics.

No evidence of the effects of 'pharmaceuticals' on Macoma balthica was found. 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. Casado-Martinez et al., 2008 examined the effects of Hg, PCB and PAH contamination on Arenicola marina but PAH and PCB sediment concentrations were not correlated with mortality. Therefore, no assessment of its sensitivity to PCBs is attempted.  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. Conti (1987) examined the effects of surfactants on Arenicola marina. The 48-hour LC50s of the two anionic detergents were 15,200 µg/l for sodium dodecyl benzene sulphonate and 12,500 µg/l for sodium dodecylbenzenesulphonate. The 48-hour LC50 of the non-ionic detergent Triton X-100 was 15,200 µg/l. Therefore, the worst-case resistance of Arenicola spp. to surfactants (detergents) is assessed as ‘Low’, resilience as ‘High’ and sensitivity assessed as ‘Low’. The confidence is assessed as ‘low’ due to the limited evidence.

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. Arenicola spp. was reported to be sensitive to several pesticides/biocides, and surfactants. 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 Arenicola marina and Macoma balthica to 'synthetic compounds' is assessed as 'None', based on the evidence from pesticide/biocide exposure in Arenicola spp.. Hence, resilience is assessed as 'Medium' and sensitivity as 'Medium'.  Where present, Cerastoderma edule is also of 'Medium' sensitivity to some 'Synthetic compounds'. 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

Reports on littoral sediment benthic communities at Sandside Bay, adjacent to Dounray nuclear facility, Scotland, (where radioactive particles have been detected and removed) reported Arenicola marina were abundant (SEPA, 2008). Kennedy et al. (1988) reported levels of ¹³⁷Cs in Arenicola spp. of 220-440 Bq/kg from the Solway Firth. Hutchins et al. (1998) described the effect of temperature on bioaccumulation by Macoma balthica (as Macoma balthica) of radioactive americium, caesium and cobalt, but made no comment on the intolerance of the species. Insufficient evidence was available on the effects of radionuclide contamination to assess this pressure. 

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.  Galloway et al. (2010) investigated the sublethal toxicity of nano-titanium dioxide and carbon nanotubes on the marine polychaete Arenicola marina. The lugworms were exposed through natural sediments to a 10-day OECD/ASTM 1990 acute toxicity test. Sediment was prepared with either single-walled carbon nanotubes (0.003–0.03 g/kg), nano-titanium dioxide (1–3 g/kg), or seawater alone. The lugworms were fed every other day and feeding behaviour was monitored every 48 hours. Casts were collected, dried overnight and weighed, with seawater renewals every 48 hours following cast collection. After 10 days of exposure, the lugworms were removed from the exposure sediment and the lugworm's ability to re-bury into clean sediment was assessed following the OECD/ICES A. marine burrowing bioassay. Sediment exposure to single-walled carbon nanotubes or nano-titanium dioxide had no effects on the burrowing behaviour of the lugworm. During the exposure period, single-walled carbon nanotubes had no effects on the feeding behaviour of the lugworms. However, nano-titanium dioxide exposure caused a significant impact on feeding behaviour with reductions in casting rate at 2 g/kg nano-titanium dioxide. Therefore, Arenicola marina is probably ‘Not sensitive’ to single-walled carbon nanotubes (at 0.003–0.03 g/kg). However, confidence in the assessment is ‘low’ due to the lack of evidence.

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 would be assessed as ‘Low’, so that 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 et al. (1975) exposed Macoma balthica to 100, 330, 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. 

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 the pressure. The sensitivity of the dominant characteristic species Arenicola marina and Macoma balthica to 'other substances' varies with the 'substance' studied, its concentration and duration of exposure.  Therefore, the worst-case resistance of this biotope to 'other substances' is assessed as ‘Medium’ based on the effects of pulverised fuel ash and wastewater on Macoma spp., resilience as ‘High’, and sensitivity as ‘Low’ but with ‘Low’ confidence. Where present, 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, the evidence on the effects of each chemical tested should be treated separately and the above species-specific assessments used where appropriate. 

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

Occurrence of dissolved oxygen concentration of less than or equal to 2 mg/l for 1 week, will reduce the oxygen availability when Arenicola marina switches back to aerobic metabolism.

Arenicola marina was able to survive anoxia for 90 hrs in the presence of 10 mmol/l sulphide in laboratory tests (Zeber & Schiedek, 1996). Hydrogen sulphide (H2S) produced by chemoautotrophs within the surrounding anoxic sediment and may, therefore, be present in Arenicola marina burrows. Although the population density of Arenicola marina decreases with increasing H2S, Arenicola marina is able to detoxify H2S in the presence of oxygen and maintain low internal concentration of H2S. At high concentrations of H2S in the lab (0.5, 0.76 and 1.26 mmol/l) the lugworm resorts to anaerobic metabolism (Zeber & Schiedek, 1996). At 16°C Arenicola marina survived 72 hrs of anoxia but only 36 hrs at 20°C. Tolerance of anoxia was also seasonal, and in winter anoxia tolerance was reduced at temperatures above 7°C. Juveniles have a lower tolerance of anoxia but are capable of anaerobic metabolism (Zebe & Schiedek, 1996). However, Arenicola marina has been found to be unaffected by short periods of anoxia and to survive for 9 days without oxygen (Borden, 1931 and Hecht, 1932 cited in Dales, 1958; Hayward, 1994).

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 survived low oxygen concentrations and shell growth continued (Jansson et al., 2015). In hypoxic conditions individual Macoma balthica moved upwards to fully expose itself on the surface of the sand or buried at shallower depths, leaving them at greater risk of predation (Long et al., 2014). 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 in to the overlying water when water was slowly deoxygenated with a stream of nitrogen. The lower the oxygen concentration became the further the siphons extended.

This behaviour, an initial increase in activity stimulated by oxygen deficiency, is of interest because the activity of lamellibranchs is generally inhibited by oxygen deficient conditions (Brafield & Newell, 1961). Dries & Theede (1974) reported the following LT50 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 and predation risk may increase. Metabolic function should quickly return to normal when oxygen levels are resumed and so recovery is expected.

Rosenberg et al. (1991) observed that Cerastoderma edule migrated to the sediment surface in response to reduced oxygen concentrations in the upper sediment layers and reported 100% mortality of Cerastoderma edule exposed to 0.5-1.0 ml/l oxygen for 43 days. Theede et al. (1969) reported 50% mortality after 4.25 days at 1.5 ml/l oxygen. Theede et al. (1969) added that Cerastoderma edule only survived 4 days’ exposure of <6.1 cm²/l of hydrogen sulphide, which is associated with anoxic conditions. Fatalities of the abundant species in the biotope, Cerastoderma edule are likely to occur at the benchmark.

During low tide the superabundant polychaete Scoloplos armiger survives de-oxygenation by ascending into the oxidative layer where it is able to maintain aerobic metabolism. In laboratory conditions Scoloplos armiger survived low oxygen conditions for 40 hours (Schöttler & Grieshaber, 1988). Limited evidence was returned by searches on extended exposure to low levels of dissolved oxygen.

Sensitivity assessment. The characterizing species of the biotope display tolerance of low dissolved oxygen over tidal cycles although some mortality may be expected at the extent of the pressure benchmark for certain species. Arenicola marina have shown tolerance for up to 9 days. Macoma balthica is likely to experience increased predation pressure as a result of extending its syphon under low oxygen conditions. Cerastoderma edule only survived 4 days’ exposure of <6.1 cm²/l of hydrogen sulphide, which is associated with anoxic conditions and is most likely to experience large scale mortality. Scoloplos armiger displays tolerance to these conditions for up to 40 hours but evidence returned by searches was limited beyond that.

Resistance is assessed as ‘Medium’, resilience is assessed as ‘High’ and therefore, 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. 

An influx of high-quality organic matter (Graf, 1989; Levin et al., 1997), may influence the distribution of species and the surrounding sediments, to support microbial communities that differ from those in the surface sediments (Kristensen & Kostka, 2005; Papaspyrou et al., 2005; Laverock et al., 2010; Braeckman et al., 2014). Additionally, bioturbators (such as Arenicola marina) may stimulate biogeochemical processes along the burrow walls resulting in an increase of nutrient fluxes to the water column (Stief, 2013). At the same time, higher coupled nitrification-denitrification rates along burrow walls give rise to an important release of nitrogen gas from the sedimentary nitrogen cycle (Stief, 2013), thereby counteracting nitrogen eutrophication (Seitzinger, 1988).

However, this biotope is considered to be 'Not Sensitive' at the pressure benchmark that assumes compliance with good status as defined by the WFD.

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 supplies, enhancing productivity and abundance. Gray et al. (2002) concluded that organic deposits between 50 to 300 g C/m²/year, is efficiently processed by the benthic species. Whilst substantial increases >500 g C/m²/year would likely to have negative effects, limiting the distribution of organisms, and degrade the habitat, by leading to eutrophication, algal blooms and changes in community structure (see nutrient enrichment and de-oxygenation) (Snelgrove & Butman, 1995; Cromey et al., 1998).

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 lead 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 resist periods of up to 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 from waste-water discharge (Dutch Wadden Sea) resulted in positive effects on Macoma balthica abundance, biomass, shell growth and production. These effects were concluded to be due to increased food supply (Madsen & Jensen, 1987). Organic enrichment, related to increased food supply has also been related to significantly increased settlement of juvenile Arenicola marina (Hardege et al., 1998).

Borja et al. (2000) assessed relative sensitivity of Scoloplos armiger as an ABMI Ecological Group II species (indifferent/tolerant to enrichment). Gittenberger & Van Loon (2011) assessed Pygospio elegans as an AMBI Group III species ‘not sensitive to organic enrichment’.

Sensitivity assessment. There is little empirical evidence to quantify the effect of organic enrichment deposits of 100 g C/m²/year on Arenicola marina and Macoma balthica but the existing studies suggest these species would not suffer negative impacts under the benchmark pressure, although deposits of greater than the benchmark (e.g. 500 g C/m²/year would negatively impact the biotope). Therefore, a resistance of ‘High’ is recorded so that resilience is also ‘High’ and the biotope is probably biotope is ‘Not Sensitive’ at the benchmark level.

Physical loss (to land or freshwater habitat)

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

Evidence

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

Physical change (to another seabed type)

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

Evidence

This biotope is only found in sediment, in particular muddy sand or fine sand the burrowing organisms, Arenicola marina, and Macoma balthica would not be able to survive if the substratum type was changed to either a soft rock or hard artificial type. Consequently the biotope would be lost altogether if such a change occurred. 

Sensitivity assessment. The resistance to this change is ‘None’, and the resilience is assessed as ‘Very Low’ as the change at the pressure benchmark is permanent. The biotope is assessed to have a ‘High’ sensitivity to this pressure at the benchmark.

Physical change (to another sediment type)

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

Evidence

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). For this biotope three adjacent categories are relevant, these include a change from muddy sand to i) sandy mud or ii) gravelly muddy sand or a change from sand to; iii) gravelly sand (Folk, 1954 cited in Long 2006).

A change to sandy mud is likely to have limited impact on the characterizing species as these conditions would remain close to preferred habitat conditions. For example, Arenicola marina displays a broad sediment habitat preference including sandy mud (Tyler-Walters, 2008). Macoma balthica prefers very fine sediments with high mud content and Scoloplos armiger sediments 200-350 µm that are enriched with mud (Degraer et al., 2006).

An increase in gravel content to either ii) gravelly muddy sand or iii) gravelly sand is likely to influence the benthic species community within the biotope. Arenicola marina displays some tolerance to increased gravel content in UK case studies, but generally abundance decreases (Chapman & Newell, 1949; King, 1980).  Macoma balthica is likely to tolerate increased gravel content as sediment was not shown to affect burrowing (Tallqvist, 2001), however, growth, shell size and body mass were greatest in higher sand content sediment and  lower in higher gravel content sediments (Azouzi et al., 2002), suggesting long-term health and abundance may be affected by long-term increased gravel content.

Coarser sediments provide inhospitable conditions for colonizing infauna. Scoloplos armiger and Pygospio elegans are opportunistic species that are capable of exploiting these inhospitable conditions (Gray, 1981). Therefore, these species are likely to be less affected and even increase in abundance under a change in Folk class from muddy sand to gravelly muddy sand or a change from sand to gravelly sand.

Sensitivity assessment. Although a change to sandy mud is likely to have limited impact a change to ii) gravelly muddy sand or iii) gravelly sand are likely to impact the characterizing species Arenicola marina and Macoma balthica. Case studies from UK sites display decreasing abundance with increased gravel content (Arenicola marina) and reduced growth rates (Macoma balthica). This suggests that the resistance is ‘None’ as abundance of these key characterizing species would possibly decrease and the biotope would alter if an increase in gravel content persisted. Resilience as Very low (the pressure is a permanent change), and sensitivity 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

The substratum of this biotope consists of fine sand or muddy sand with scattered pebbles, boulders and cobbles (Conner et al., 2004). The characterizing species Arenicola marina and Macoma balthica burrow into the sediment, to depths not exceeding 30 cm. The process of extraction is considered to remove all biological components of the biotope group. If extraction occurred across the entire biotope, loss of the biotope would occur. Recovery would require substratum to return to fine sand and muddy sand sediments with scattered pebbles, boulders and cobbles. Recovery of benthic infauna communities from an impact such as extraction of substratum (from activities such as use of bottom towed fishing gears, aggregate dredging or storm impacts) is predicted to follow succession from initial colonization community of opportunistic species that reproduce rapidly, have small body sizes, short lifespans and early reproductive ages, through to a transitional community and finally an equilibrium community of slower growing, longer lived, larger species (Newell et al., 1998). 

Arenicola marina and Macoma balthica are more likely to occur in the late transitional and the equilibrium communities that rely on more stable sediments that have recovered from disturbance (Newell et al., 1998). Therefore, even if hydrological conditions allow for re-establishment of fine sand and muddy sand, recovery times to an equilibrium community, from an impact such as dredging are predicted to be between 2-3 years minimum and often 5-10 years (Newell et al., 1998).

Hiddink (2003) showed that the density of Macoma balthica was reduced in areas in the Wadden Sea (Netherlands) that had experienced suction dredging for cockles, which removes the surface sediment. The disturbance to the sediment also appeared to leave the habitat less suitable for settlement of young Macoma balthica (Hiddink, 2003).

Smaller scale extraction of patches of substratum through activities such as bait digging may have impacts over finer spatial scales within the biotope. If the impact is not spread over a larger area the effects are likely to occur within the dug area. McLusky et al. (1983) found that Arenicola marina rapidly recolonise basins created by bait digging but populations were reduced in the dug mounds. Macoma balthica populations were unaffected suggesting the biotope would recover from this impact if it occurred over a limited spatial scale.  

Sensitivity assessment. Resistance to extraction of substratum to 30 cm across the entire biotope is assessed as ‘None’ based on expert judgment, but supported by the literature relating to the position of these species on or within the seabed and literature on impacts of dredging and bait digging activities.  At the pressure benchmark, the exposed sediments are considered to be suitable for recolonisation almost immediately following extraction.  Recovery will be mediated by the scale of the disturbance and the suitability of the sedimentary habitat. Recovery is most likely to occur via larval recolonization, following a succession from colonization communities to equilibrium communities only after 2-10 years (not including time for sediment to recover). Resilience is considered to be ‘Medium’. Sensitivity based on resistance and resilience is therefore categorized as ‘Medium’.

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

Damage to seabed surface features may occur due to human activities such as bottom towed fishing gear (trawling and dredging), construction of renewable energy devices offshore and natural disturbance from storms are considered in this assessment.The burrowing traits of Arenicola marina and Macoma balthica may provide some resistance to this pressure. However, Boldina & Beninger (2014) reported decreases in naturally occurring aggregations of Arenicola marina in trawled areas, which suggests consequences reproduction, recruitment, growth and feeding.

Ferns et al. (2000) reported a decline of 31% in populations of Scoloplos armiger (initial density 120/m²) in muddy sands and an 83% decline in Pygospio elegans (initial density 1850/m²) when a mechanical tractor towed harvester was used (in a cockle fishery). Pygospio elegans were significantly depleted for >100 days after harvesting (surpassing the study monitoring timeline).

Scoloplos armiger demonstrated recovery >50 days after harvesting in muddy sands. Cerastoderma edule recovered more quickly than those in muddy sand with a more structured community, which included Pygospio elegans in clean sands (Ferns et al., 2000).

Collie et al. (2000) identified that well established sand and muddy sand intertidal communities (such as this biotope) suffered the greatest impact from bottom towed fishing activities. Mean response in muddy sand communities was much more negative than other habitats and most negative responses were for the polychaetes Arenicola marina and Scoloplos armiger. Macoma balthica and Cerastoderma edule were also more negatively impacted, although this may be due to direct targeting of Cerastoderma edule by cockle fisheries. The review concluded that there were ecologically important impacts from removal of >50% of fauna from bottom towed fishing activity (dredge and trawls) (Collie et al., 2000).

Construction of offshore wind farms or deployment of wave energy device bases are likely to remove the biotope at the site of the wind farm tower or concrete wave energy base. Drilling and piling during construction will also re-suspend sediment into the water column, with coarser material settling close to the base and finer material being deposited at a greater distance in the direction of water flow at the site (Coates et al., 2014). Pre-existing characterizing communities will be impacted and a risk of recovery to a different equilibrium community may occur (Newell et al., 1998; Coates et al., 2014; Coates et al., 2015).

Changes in sediment, close to device bases, will prevent the establishment of this biotope and finer sediment is likely to be deposited close to a device base in the wake of the main current (Coates et al., 2014). In a case study in the Belgium North Sea, this process resulted in shifts in species dominance to tube building polychaetes (which may stabilise fine sediments), this impact was highest within 15 m of device bases (Coates et al., 2014). Where scour protection is not present, coarser material may be exposed adjacent to device bases and finer material that has been removed by scour, deposited along the wake of the main current (Hiscock, 2002). Shifts in species communities and dominant species occur in both examples but are limited to 15 m to 20 m from the device bases.

Boat moorings were demonstrated to also impact species communities close to the mooring buoy in a case study in the Fal and Helford estuaries (south west UK). Coarser sediment was exposed close to mooring buoys, caused by suspension of fine sediments by movement of the chain (Latham et al., 2012). However, fine sand and muddy sediments displayed the least influence from disturbance from moorings, suggesting a smaller impact to this biotope than other intertidal biotopes.

Sensitivity assessment.  Resistance is ‘Low’ as significant mortality of characterizing species was recorded in the above evidence. Resilience is ‘Medium’ if the impact is less than 3 times a year, as recovery is expected in 2-10 years based on the life cycle traits of the characterizing species. Sensitivity for occasional (less than 3 times a year) damage to the seabed surface features is therefore ‘Medium’ at the benchmark level.

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

Penetration and or disturbance of the substratum would result in similar, if not identical results as ‘abrasion’ or ‘removal’ of this biotope. As the characterizing species are burrowing species the impact from damage to the sub-surface sea bed would be greater than damage to the sea bed surface.

Sensitivity assessment. Resistance of the biotope is assessed as ‘Low’, although the significance of the impact for the bed will depend on the spatial scale of the pressure footprint. Resilience is assessed as ‘Low’, and sensitivity is assessed as ‘High’.

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

Changes in light penetration or attenuation associated with this pressure are not relevant to Arenicola marina and Macoma balthica biotopes. As the species live in the sediment they are also likely to be adapted to increased suspended sediment (and turbidity). However, alterations in the availability of food or the energetic costs in obtaining food or changes in scour could either increase or decrease habitat suitability for Arenicola marina, Macoma balthica as characterizing species and for other abundant species such as Scoloplos armiger, Pygospio elegans and Cerastoderma edule.

Increases in turbidity may reduce benthic diatom productivity and productivity of phytoplankton in the water column. Increased clarity, however, may increase primary production. In cases of increased turbidity impacts may be small for Arenicola marina as the species feeds on meiofauna, bacteria and organic particles in the sediment and reductions in food availability in phytoplankton may be mitigated.    

An increase in suspended solids (inorganic or organic) may also increase food availability if sediment containing meiofauna, bacteria or organic particles is transported in the water column. However, higher energetic expenditure to unclog the feeding apparatus may occur, which may alter habitat suitability.

An increase in food availability through either increased phytoplankton abundance (under increased water clarity) or increased food resources suspended in the water column (under increased turbidity) may enhance growth and reproduction of both suspension and deposit feeding species.

Sensitivity assessment. Resistance is ‘High’ as no significant negative effects are identified and potential benefits from increased food resources may occur, based on expert judgement, utilising evidence of species traits and distribution. Resilience is also ‘High’ as no recovery is required under the likely impacts. Sensitivity of the biotope is, therefore assessed as ‘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

The biotope occurs in extensive intertidal flats both on open coasts and in marine inlets (Conner et al., 2004). These locations would be likely to experience some redistribution of fine material during tidal cycles. Although the biotope occurs in sheltered locations some mixing from wave action may also be expected. The characterizing species Arenicola marina and Macoma balthica live in the sediment, to depths of 40 cm and 5-6 cm respectively (Stekoll et al., 1980; Volkenborn & Reise, 2006) and would be expected to be well adapted to these conditions.

Longer term deposition of fine material (e.g. continuous deposition) would be expected to lead to higher densities of macrobenthic organisms. For example, in the North Sea (Belgium) deposition of fine particle sediment, disturbed by scour around the base of a wind farm tower led to higher macrobenthic densities and created a shift in macrobenthic communities around the wind farm tower (influenced by the  direction fine material had settled) (Coates et al., 2014).

Sensitivity assessment. As the exposure to the pressure is for a single discrete event, resistance is assessed as ‘High’, resilience is also ‘High’ and sensitivity is assessed as ‘Not Sensitive’. Confidence in this assessment is lower as the assessment is based on traits of the species characterizing the biotope and the relevant direct case studies present examples where impacts are not from single discrete events. 

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

Limited evidence was found on responses of characterizing species to a deposition of up to 30 cm of fine material. Evidence is therefore assessed for evidence of deposits of fine material from sources such as dredge waste spoil and bait digging mounds (which may not be 30 cm).

Smaller scale extraction of patches of substratum through activities such as bait digging may have impacts over finer spatial scales within the biotope. If the impact is not spread over a larger area the effects are likely to occur within the dug area. McLusky et al. (1983) found that Arenicola marina rapidly recolonise basins created by bait digging but populations were reduced in the dug mounds, suggesting the species would be negatively impacted by heavy deposition of sediment. Macoma balthica populations were unaffected by bait digging suggesting the species can re-colonise areas where heavy deposition of sediment has occurred.

Witt et al. (2004) identified an increased in Macoma balthica populations in areas of disposal of dredge waste spoil, possibly due to nutrient input at the disposal site. This suggests Macoma balthica responds opportunistically and is robust to this pressure.

Cerastoderma edule on the north Norfolk coastline was shown to be severely depleted from the effects of bait digging, as a result of 10 cm of sediment being placed on the sediment surface (Jackson & James, 1979; McLusky et al., 1983; Cryer et al., 1987). Small, surface-dwelling, polychaete species have been shown to be compromised by changes to sediment structure as a result of heavy muddy sediment spoil from bait digging (Brown et al., 1997). This has the potential to disturb the species composition and the abundance of opportunistic species may increase, negatively impacting the biotope.

Pygospio elegans was classified as ‘Group III’ by Borja et al. (2000) as tolerant of disturbance and excess organic content. As a tube building worm, Pygospio elegans also stabilises sediments, a trait which aids recolonization of disturbed sediments or deposited material (Bolam & Fernandes, 2002).

Longer term or heavy deposition of fine material (e.g. continuous deposition) would be expected to lead to higher densities of macrobenthic organisms. For example, in the North Sea (Belgium) deposition of fine particle sediment, disturbed by scour around the base of a wind farm tower led to higher macrobenthic densities and created a shift in macrobenthic communities around the wind farm tower (in the direction fine material had settled) (Coates et al., 2014).

Sensitivity assessment. Deposition of up to 30 cm of fine material is likely to provide different impacts for the different species characterizing the biotope. Overall, though the pressure is likely to negatively impact the biotope as the characterizing species Arenicola marina may experience reduced abundance. Macoma balthica and the polychaete Pygospio elegans are likely to be able to exploit the increased nutrient input and rapidly colonize the deposited sediment.

Other opportunistic species are likely to colonize the biotope if heavy deposition of fine material occurs. The deposited sediment is likely to release large quantities of organic materials enhancing population density but with the risk that pre-impacted communities will shift to a different state (Coates et al., 2014; Coates et al., 2015). Recovery to pre-impact communities, given the pressure occurs as a single discrete event is likely to require succession through transitional communities before an equilibrium community is reached, taking up to 10 years (Newell et al., 1998).

Resistance is assessed as ‘Low’, due to loss of abundance of at least one characterizing species. Resilience is assessed as ‘Medium’ as recovery may take 2-10 years. The final sensitivity is therefore ‘Medium’. 

Litter

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

Evidence

Litter, in the form of cigarette butts, has been shown to have an impact on worms living in the sediment, although effects have not been studied directly on species characterizing this biotope. Ragworms Hediste diversicolor, which also inhabit intertidal sediments showed increased burrowing times, 30% weight loss and a > 2-fold increase in DNA damage when exposed to water with toxicants (present in cigarette butts) in quantities 60-fold lower than reported from urban run-off (Wright et al., 2015). Studies are limited on impacts of litter on infauna and this UK study suggests health of infauna populations are negatively impacted by this pressure.

Arenicola marina ingests microplastics that are present within the sediment it feeds within. Wright et al. (2013) carried out a lab study that displayed presence of microplastics (5% UPVC) significantly reduced feeding activity when compared to concentrations of 1% UPVC and controls. As a result, Arenicola marina showed significantly decreased energy reserves (by 50%), took longer to digest food, and as a result decreased bioturbation levels, which would be likely to impact colonization of sediment by other species, reducing diversity in the biotopes the species occurs within. Wright et al. (2013) suggested, that in the intertidal regions of the Wadden Sea, where Arenicola marina is an important ecosystem engineer, Arenicola marina could ingest 33 m² of microplastics a year.

Sensitivity assessment. Impacts from the pressure ‘litter’ would depend upon the exact form of litter or man-made object being introduced. In the case of marine litter in the form of cigarette butts or microplastics health of populations of characterizing species would be impacted. Significant impacts have been shown in laboratory studies but impacts at biotope scales are still unknown and this pressure is  ​Not assessed.

Electromagnetic changes

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

Evidence

Electric and magnetic fields generated by sources such as marine renewable energy device/array cables may alter behaviour of predators and affect infauna populations. Evidence is limited and occurs for electric and magnetic fields below the benchmark level, confidence in evidence of these effects is low.

Field measurements of electric fields at North Hoyle wind farm, North Wales recorded 110 µV/m (Gill et al., 2009). Modelled results of magnetic fields from typical subsea electrical cables, such as those used in the renewable energy industry produced magnetic fields of between 7.85 and 20 µT (Gill et al., 2009; Normandeau et al., 2012). Electric and magnetic fields smaller than those recorded by in field measurements or modelled results were shown to create increased movement in thornback ray Raja clavata and attraction to the source in catshark Scyliorhinus canicular (Gill et al., 2009).

Flatfish, which are predators of many polychaete species, including dab Limanda limanda and sole Solea solea have been shown to decrease in abundance in a wind farm array or remain at distance from wind farm towers (Vandendriessche et al., 2015; Winter et al., 2010). However, larger plaice increased in abundance (Vandendriessche et al., 2015). There have been no direct causal links identified to explain these results.

However, there is not enough evidence to assess the sensitivity of the characterizing species and sediments to litter.  

Underwater noise changes

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

Evidence

Species within the biotope can probably detect vibrations caused by noise and in response may retreat in to the sediment for protection. However, at the benchmark level the community is unlikely to be respond to noise and therefore is 'Not relevant'.

Introduction of light or shading

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

Evidence

There is no direct evidence of effects of changes in incident light on the characterizing species of this biotope. All characterizing species live in the sediment and do not rely on light levels directly to feed or find prey so limited direct impact is expected.  As this biotope is not characterized by the presence of primary producers it is not considered that shading would alter the character of the habitat directly.

More general changes to the productivity of the biotope may, however, occur. Beneath shading structures there may be changes in microphytobenthos abundance. Littoral muddy sands support microphytobenthos on the sediment surface and within the sediment. The microphytobenthos consists of unicellular eukaryotic algae and cyanobacteria that grow within the upper several millimetres of illuminated sediments, typically appearing only as a subtle brownish or greenish shading. Mucilaginous secretions produced by these algae may stabilise fine substrata (Tait & Dipper, 1998).

Shading will prevent photosynthesis leading to death or migration of sediment microalgae altering sediment cohesion and food supply to higher trophic levels. The impact of these indirect effects is difficult to quantify.

Sensitivity assessment. Based on the direct impact, biotope resistance is assessed as ‘High’ and resilience is assessed 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

'Not relevant'. This pressure is considered applicable to mobile species, e.g. fish and marine mammals rather than seabed habitats. Physical and hydrographic barriers may limit the dispersal of seed.  But seed dispersal is not considered under the pressure definition and benchmark.

Barriers that reduce the degree of tidal excursion may alter larval supply to suitable habitats from source populations. Barriers may also act as stepping stones for larval supply over greater distances (Adams et al., 2014). Conversely, the presence of barriers in brackish waters may enhance local population supply by preventing the loss of larvae from enclosed habitats to environments, which are unfavourable, reducing settlement outside of the population. If a barrier (such as a tidal barrier) incorporated renewable energy  devices such as tidal energy turbines, these devices may affect hydrodynamics and, therefore, migration pathways for larvae into and out of the biotope (Adams et al., 2014). However, evidence is limited.

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 interaction with bottom towed fishing gears and moorings are 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

Arenicola marina larvae and the other associated polychaete species may have some limited visual perception. As they live in the sediment the species will most probably not be impacted at the pressure benchmark.

Sensitivity assessment.  As the characterizing species live within the sediment and are likely to have limited visual perception this pressure is assessed as ‘Not relevant’.

Genetic modification & translocation of indigenous species

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

Evidence

Key characterizing species within this biotope are not cultivated or translocated. Therefore, this pressure is considered ‘Not relevant’ to this biotope group.

Introduction or spread of invasive non-indigenous species

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

Evidence

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 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). 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 (Herbert et al., 2012). 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%).

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 levels to the shallow subtidal (Troost, 2010; 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 a decrease in settlement space and a 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.

Sensitivity assessment. 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). However, scattered stones and cobbles may occur in examples of this biotope that may allow localized colonization by Crepidula at low densities but it is unclear if this would expand to the rest of the biotope. In addition, despite the extremely sheltered conditions of the habitat that would otherwise be suitable for Crepidula, the mobility of the sediment is unsuitable and it is unlikely Crepidula would 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). No direct evidence relating to the detrimental impacts of the introduction of non-indigenous species was found for Arenicola marina or Macoma balthica. Therefore, resistance to colonization by Crepidula fornicata is assessed as 'High' and resilience as 'High' so the biotope is assessed as 'Not sensitive'. 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 the biotope. Further evidence is required. 

The above evidence suggests that this biotope is unsuitable for the colonization of Magallana gigas 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). However, scattered stones and cobbles may occur in examples of this biotope that may allow localized colonization by Magallana gigas at low densities but, there might not be sufficient hard substrata for colonization and establishment, limiting the Pacific oyster to lower densities. In addition, evidence has suggested the distribution of Magallana gigas can overlap with Macoma balthica and other native bivalve species (Troost, 2010; Herbert et al., 2012, 2016). 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 (Troost, 2010; Herbert et al., 2012, 2016). However, the oyster could colonize the lower shore extent or examples of the biotope in higher densities. Therefore, a precautionary resistance to colonization by Magallana gigas of  'Medium' is suggested. 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

'No evidence' on the effect on Arenicola marina of introduction of relevant microbial pathogens or metazoan disease vectors was found.

Macoma balthica in Delaware Bay, north-east USA, was found to host Perkinsus genus pathogens (Lindsay et al., 2007). Cerastoderma edule has been reported to host approximately 50 viruses, bacteria and fungi, including turbellaria, digeneans and cestodes (Longshaw & Malham, 2012). Bacterial diseases are more significant in the larval stages and protozoans are the most common cause of epizootic outbreaks leading to mass mortalities of bivalves. Parasitic worms, trematodes, cestodes and nematodes can reduce growth and fecundity in bivalves and may in some instances cause death (Dame, 1996). Cerastoderma edule may be infected by numerous larval digenean trematodes and the parasitic copepod Paranthessius rostatus but no evidence of mass mortalities of cockles in the British Isles attributable to parasites was found. Boyden (1972) reported castration in cockles by parasites from the River Couch estuary, Essex, potentially reducing subsequent population sizes.

Mortality rates in the commercial Cerastoderma edule fishery in Galicia (NW Spain) increased sharply in April 2012, reaching 100% by May. Marteiliosis, which was first detected in February 2012 and reached 100% prevalence in April 2012, was identified as the most probable cause. Extensive surveillance of the Galician coast in May to July 2012 detected marteiliosis in most cockle beds of the Ría de Arousa, whereas it was not found in other rías 2 months later, the cockle catch in the Ría de Arousa became negligible as a result of a Martelia cochillia protozoan infection (Villalba et al., 2014). There is insufficient information to assess the recoverability of Cerastoderma edule and parasitic infection by Martelia cochillia and other related protozoan species such as Martelia refringens, which affects European bivalves (Carrasco et al., 2012).

Sensitivity assessment. Based on the evidence for the Cerastoderma edule, it is likely that parasitic infection may indirectly alter the species composition of the biotope. Although less evidence was retuned for the characterizing mollusc species Macoma balthica.  Although evidence and so confidence is limited, resistance is assessed as ‘Medium’, resilience is assessed as ‘High’ and sensitivity is therefore assessed as ‘Low’.

Removal of target species

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

Evidence

Fowler (1999) reviewed the effects of bait digging on intertidal fauna, including Arenicola marina. Diggers have been reported to remove 50 or 70% of the blow lug population. Heavy commercial exploitation in Budle Bay in winter 1984 removed 4 million worms in 6 weeks, reducing the population from 40 to <1 per m². Recovery occurred within a few months by recolonization from surrounding sediment (Fowler, 1999). However, Cryer et al. (1987) reported no recovery for 6 months over summer after mortalities due to bait digging. Mechanical lugworm dredgers have been used in the Dutch Wadden Sea where they removed 17-20 million lugworm/year. A near doubling of the lugworm mortality in dredged areas was reported, resulting in a gradual substantial decline in the local population over a 4 year period. The effects of mechanical lugworm dredging is more severe and can result in the complete removal of Arenicola marina (Beukema, 1995; Fowler, 1999). Beukema (1995) noted that the lugworm stock recovered slowly reaching its original level in at least three years. McLusky et al. (1983) examined the effects of bait digging on blow lug populations in the Forth Estuary. Dug and infilled areas and unfilled basins left after digging re-populated within 1 month, whereas mounds of dug sediment took showed a reduced population. Basins accumulated fine sediment and organic matter and showed increased population levels for about 2-3 months after digging. Overall, recovery is generally regarded as rapid. However, Fowler (1999) pointed out that recovery may take longer on small pocket beaches with limited possibility of recolonization from surrounding areas. Therefore, if adjacent populations are available, recovery will be rapid. However, where the affected population is isolated or severely reduced (e.g. by long-term mechanical dredging), then recovery may be extended.

Smaller scale extraction of patches of substratum through activities such as bait digging may have impacts over finer spatial scales within the biotope. If the impact is not spread over a larger area the effects are likely to occur within the dug area. McLusky et al. (1983) found that Arenicola marina rapidly re-colonize basins created by bait digging but populations were reduced in the dug mounds. Macoma balthica populations were unaffected in dug areas, suggesting the biotope would recover from this impact if it occurred over a limited spatial scale.  

Hiddink (2003) showed that the density of Macoma balthica was reduced in areas in the Wadden Sea (Netherlands) that had experienced suction dredging for cockles, which removed the surface sediment. The disturbance to the sediment also appeared to leave the habitat less suitable for settlement of young Macoma balthica (Hiddink, 2003). This study provides evidence of loss of a characterizing species from the biotope and that recovery is unlikely to occur until the sediment characteristics have returned to pre-impact conditions. Removal of target species such as cockles Cerastoderma edule or bait digging for Arenicola marina is likely to impact the biotope. The extent of the impact will depend on the fishing / removal method and spatial extent.

Sensitivity assessment. Arenicola marina re-colonize basins created by bait digging but increased recovery times for larger scale mechanical dredging have been reported to occur (up to 3 years). Macoma balthica populations were unaffected by manual bait digging but were reduced in areas in the Wadden Sea (Netherlands) that had experienced suction dredging for cockles, which removes the surface sediment. The following sensitivity assessment therefore considers the greater impact, from commercial scale mechanical dredging (lugworm) or suction dredging (cockles). Resistance is assessed as ‘Low’ and resilience is assessed as ‘Medium’ (for cases where removal is large scale, e.g. mechanical dredging where recovery can take up to 3 years). Therefore, sensitivity to large scale mechanical or suction dredging is therefore assessed as ‘Medium’.

Removal of non-target species

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

Evidence

Direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures, while this pressure considers the ecological or biological effects of by-catch. Species in these biotopes, including the characterizing species, Arenicola marina and Macoma balthica as well as the abundant species: Scoloplos armiger and Pygospio elegans, Tubificoides benedii and Tubificoides pseudogaster, and the cockle Cerastoderma edule, may be damaged or directly removed by static or mobile gears that are targeting other species (see abrasion and penetration pressures).

Commercial fisheries may discard damaged or dead non-target species, which could result in increased available food supply to deposit feeding characterizing species that may have survived in the area targeted by fisheries, but may also attract mobile predators and scavengers including fish and crustaceans which may alter predation rates in the biotopes.

Sensitivity assessment. The intertidal fine and muddy sand sediments present in this biotope are targeted by dredge fisheries for cockles and commercial bait digging and mechanical dredging for lugworms. Otter trawling and beam trawling is also possible in deeper areas at high water. Species recovery rates range from up to 3 years for Arenicola marina impacted by large scale mechanical dredging and >50-100 days for superabundant polychaete species removed incidentally.

Resistance is assessed as ‘Low’ (for cases where significant mortality/extraction of key characterizing species occurs), Resilience is assessed as ‘Medium’ (for cases where removal is large scale, e.g. mechanical dredging where recovery can take up to 3 years) and sensitivity to incidental non-targeted catch is therefore assessed as ‘Medium’.