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

Hediste diversicolor and other important characterizing species are adapted to living within the intertidal zone where temperatures fluctuate. Some resistance to temperature fluctuations is achieved by burying within the sediment, which buffers against acute temperature changes over the tidal cycle. the sensitivity assessment for this pressure is largely based on geographic range as a proxy for thermal tolerances, laboratory experiements and field observations.

The geographic range of Hediste diversicolor (throughout north-west Europe on the Baltic Sea, North Sea and along Atlantic coasts to the Mediterranean) suggests that it is tolerant of a range of temperatures and a temperature increase at benchmark levels is unlikely to have an adverse effect on UK populations. Hediste diversicolor can tolerate temperatures from below zero under Baltic ice to high summer temperatures in Black Sea lagoons (>25°C) (Smith, 1977). Hediste diversicolor were not strongly affected by heat waves in an estuary in north western Portugal, where temperatures reached 40°C in intertidal pools (higher temperatures than experienced around UK and Irish coasts) (Dolbeth et al., 2011). Grilo et al., 2011) found that at a Portuguese site, surface deposit feeders gradually decreased in periods of higher temperatures. However, sub-surface deposit feeders became dominant for up to three years after heat wave conditions had passed.

Temperature change may adversely affect reproduction of Hediste diversicolor. Bartels-Hardege and Zeeck (1990) demonstrated that an increase from 12°C and maintenance of water temperature at 16°C induced reproduction in Hediste diversicolor specimens outside the normal period of spawning, and without a drop in temperature to simulate winter conditions the spawning period was prolonged and release of gametes was not synchronized. Poor synchronization of spawning could result in reduced recruitment, as gametes are wasted and mature specimens die shortly after gamete release.

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 6 hours of exposure to temperatures up to 37.5°C with no mortality. Wilson (1981) show that the lethal temperatures for Macoma balthica change between seasons as individuals acclimate to seasonal changes. Critical temperatures were studied for a Macoma balthica population in Dublin Bay, and a summer maximum of 37.5 and winter maximum of 27.5 were reported (Wilson, 1981).  Tolerances were also reported to change with height up the shore, which suggested adaptation to prevailing conditions.

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

Despite apparent adaptation to regional temperature ranges, Barda et al. (2014) studied populations of Macoma balthica in the Baltic Sea and found that increased temperature reduced growth rates. 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 in the Spanish coast along the Bay of Biscay over the past 40 years 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. Repeated recruitment failure also occurred after mild winters in a comparable North Sea location, probably due to enhanced survival of predators(Beukema, 1992, Schueckel & Kroencke, 2013; Beukema et al., 2001).  As a result, Jansen et al. (2007) predict the southern limit of the species will progressively shift north if temperatures continue to rise.

Corophium volutator is widely distributed in the north Atlantic, American and European coasts; from western Norway to the Mediterranean and the Black Sea and Azov Sea (Neal & Avant, 2006). The amphipod is subject to temperatures of 1°C in the winter to 17°C in the summer (Wilson & Parker, 1996) but can resist much higher temperatures (Meadows & Ruagh, 1981).

Pygospio elegans also shows a relationship between timing of reproduction and temperature. Gibson and Harvey (2000) in a study on asexual reproduction of Pygospio elegans in Nova Scotia, Canada found that temperature did not influence reproduction strategy (planktotrophy, lecithotrophy or asexual reproduction) but cite Anger (1984) that environmental conditions including temperature, influence the timing of reproduction.

Tubificoides benedii increased in abundance in mudflat habitats in Jade Bay, North Sea between 1930 and 2009 (Schueckel & Kroencke, 2013). Climate warming as well as decreasing nutrient loads and species introductions have occurred in the region since the 1970s, suggesting the species may adapt to temperature increases at benchmark pressures.Bamber & Spencer (1984) observed that Tubificoides were dominant species in an area affected by thermal discharge in the River Medway estuary.  Sediments were exposed to the passage of a temperature front of approximately 10^oC between heated effluent and estuarine waters during the tidal cycles. Increased temperature was found to trigger the onset of reproduction in Baltidrilus costata (studied as Tubifex costatus) in the Thames (Birtwell & Arthur, 1980). This effect was non-lethal and may be beneficial to populations.

Streblospio shrubsolii have been shown to reproduce in a temperature range of 7.5°C – 30°C with highest reproduction levels occurring between 16°C – 21°C (Levin & Creed, 1986, Dafonsecagenevois & Cazaux, 1987, Chu & Levin, 1989, Lardicci et al., 1997). The evidence  was based on Mediterranean sites, limiting confidence for UK and Irish seas. The timing of reproduction and growth, although occurring throughout the year, increased in late spring and early summer but were strongly reduced during periods of higher temperatures in summer and disappeared or were strongly reduced at lower temperatures in winter (Lardicci et al., 1997). The timing of growth and reproduction in Streblospio shrubsolii depended on the synergistic effects of temperature and photoperiod, so that cues may differ at locations at different latitudes (Chu & Levin, 1989). Both a 5°C increase in temp for one month period, or 2°C for one year are within the temperature range reproduction occurs within (7.5°C – 30°C) and within the temperature range where highest reproduction levels occur (16°C – 21°C), suggesting limited impact from the pressure at benchmark pressures is likely.  

Indirect effects are also possible. Higher temperatures have been implicated in the proliferation of trematode parasites which have caused mass mortalities in the snail Hydrobia ulvae (Jensen & Mouritsen, 1992), which is often abundant in this biotope.

Sensitivity assessment. Typical surface water temperatures around the UK coast vary, seasonally from 4-19°C (Huthnance, 2010). It is likely that the important characteristic species are able to resist a long-term increase in temperature of 2°C and may resist a short-term increase of 5°C. Macoma balthica may retreat north as a result of long-term warming and climate change. However, the important characterizing species Hediste diversicolor are likely to survive a 5°C increase in temp for one month period, or 2°C for one year, although reproductive activities may be impacted. For instance, without colder winters spawning may not be synchronised and so recruitment would be reduced. A resistance of ‘High’, a resilience of ‘High’ (as longer lived later maturing species are present) and a sensitivity of ‘Not sensitive’ have been assigned.

Temperature decrease (local)

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

Evidence

A decrease in temperature has been shown to be indirectly beneficial to Hediste diversicolor, as case studies report a reduction in numbers of the species’ predators. For instance, a severe winter in the Wadden Sea in 1995/1996 saw an increased abundance of Hediste diversicolor coincident with a reduction in the numbers of Carcinus maenus and Crangon crangon (Armonies et al., 2001). A similar increase in abundance was noted in the same area between 1978 and 1987 after a series of cold winters (mean Hediste diversicolor density increased from 24/m² to 151/m² respectively ) (Beukema, 1990). Decreased temperatures throughout the year may, however, limit reproduction. Bartels-Hardege & Zeeck (1990) induced spawning in the laboratory, in specimens of Hediste diversicolor from tidal flats of the Jadebusen (North Sea), outside the normal spawning period of early spring. Temperatures were not lowered to simulate winter conditions but maintained at 16°C. Mature specimens appeared after four weeks and released gametes after a further four weeks according to a semilunar cycle. Reproduction was sustained for a period of four months. Such an extended spawning was witnessed on the Jadebusen following an unusually warm winter. Spawning occurred from February until May and was less synchronized. In contrast, the same population spawned within two months (February - March) following lower winter temperatures in another year. They concluded that not only a threshold temperature was important for synchronized spawning but the timing of the rise in temperature following winter was also a significant factor (Bartels-Hardege & Zeeck, 1990). A reduced rise in temperature is likely to limit this factor.

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, resist much lower temperatures than it experiences in Britain and Ireland. Furthermore, Macoma balthica was apparently unaffected by the severe winter of 1962/3, which severely affected  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 likely, therefore, that in seas around the UK and Ireland,Colder winter temperatures have been shown to benefit Macoma balthica population dynamics. Recruitment success increased following colder winters and repeated recruitment failure has occurred after mild winters in comparable North Sea location (Beukema, 1992, Schueckel & Kroencke, 2013; Beukema et al., 2001). In Friedrichskoog, Germany, König (1943) found a high accumulation of dead Cerastoderma edule biomass after a severe winter 1936/1937 but high numbers of Macoma balthica (80,000 individuals/m²) spat in following years (winter 1939). Winter water surface temperatures in the Wadden Sea (Netherlands) have increased 1.5°C since the 1980s (Oost et al., 2009). During milder winters greater body weight loss and production of fewer and smaller eggs has been observed in Macoma balthica (van der Meer et al., 2003). It is noted in the literature however, that reduced recruitment success during milder winters may also be due to increased predation as juvenile Crangon crangon have shown increased abundance in relation to milder winters (Beukema & Dekker, 2005).  Macoma balthica would resist decreases in temperature at the pressure benchmark level.

Corophium volutator is subject to temperatures of 1°C in the winter to 17°C in the summer (Wilson & Parker, 1996). The population may reduce activity and delay reproduction if the temperature drops below 7°C. Sudden pulses of very cold water can disrupt the circa-tidal rhythms of Corophium volutator by resetting the onset of swimming behaviour. For example, a 6 hour cold spell would lead to the population trying to swim at low tide and leave them vulnerable to increased predation. However, it took temperatures of 15-20°C below ambient temperature to induce this response (Holmström & Morgan, 1983b).

Streblospio shrubsolii has been shown to reproduce in a temperature range of 7.5°C – 30°C with highest reproduction levels occurring between 16°C – 21°C (Levin & Creed, 1986, Da Fonseca-Genevois & Cazaux, 1987, Chu & Levin, 1989, Lardicci et al., 1997). Reproductive activity disappeared or strongly reduced at lower temperatures in winter in a Mediterranean case study (Lardicci et al., 1997), this case study suggests reproduction would be delayed in UK and Irish populations that experienced both a  5°C decrease in temp for one month period, or 2°C for one year.

Most littoral oligochaetes, including tubificids and enchytraeids, can survive freezing temperatures and can survive in frozen sediments (Giere & Pfannkuche, 1982). Tubificoides benedii (studied as Peloscolex benedeni) recovered after being frozen for several tides in a mudflat (Linke, 1939).

Sensitivity assessment. The important characterizing species show limited impacts and, potentially, benefits to abundance and recruitment from decreases in temperature. Therefore, a 5°C decrease in temp for one month period, or 2°C for one year is likely to have limited negative impact on all characterizing species in the biotope, within British and Irish seas. Hence, resistance is assessed as ‘High’, resilience is assessed as ‘High’, and sensitivity as ‘Not Sensitive’.

Salinity increase (local)

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

Evidence

The sub-biotopes; LS.LMx.GvMu.HedMx.Mac, LS.LMx.GvMu.HedMx.Scr, LS.LMx.GvMu.HedMx.Str, LS.LMx.GvMu.HedMx.Cir, LS.LMx.GvMu.HedMx.Cvol occur in reduced (18-30 ppt) or variable (18-35 ppt) salinity, whereas LS.LMx.GvMu.HedMx.Scr occurs in full salinity (30-35 ppt) (JNCC, 2015). It is noted that there are relatively few records in each sub-type, leading to uncertainty over the precise nature of the habitat, regarding salinity regime and other factors (JNCC, 2015). As most examples of this biotope occur in reduced or variable salinity the change in salinity assessed as the benchmark is to full salinity (30-35 ppt). The available evidence (summarised below) suggests that the characterizing species are tolerant of an increase to full salinity.  The restriction of this biotope to variable or reduced salinity is most likely due to the requirement for shelter from wave action rather than salinity regime.

As higher salinity examples of sheltered muddy gravels tend to be more species rich than lower salinity, upper estuarine habitats (Maddock, 2008), it is likely that an increase in salinity at the pressure benchmark will lead to an increase in species richness. An increase at the pressure benchmark may, therefore, lead to the development of the variant sub-biotope LS.LMx.GvMu.HedMx.Scr that occurs in full salinity, or the biotope mayclassification may not change but be more species rich (where wave action and flows do not increase).

Hediste diversicolor, the key characterizing species, occurs across all variant sub-biotopes and as such is resistant to the salinity range, from reduced to full, that the various sub-biotopes occur within. Hediste diversicolor is a euryhaline species, able to tolerate a range of salinities from fully marine  seawater down to 5 psu or less (Barnes, 1994).  Macoma balthica is found in brackish and fully saline waters, although it is more common in brackish waters (Clay, 1967b) so may tolerate variable saliniity. Seitz (2011) found that the distribution of Macoma balthica across a salinity gradient between a minimum and maximum of 8.8psu to 19 psu in Cheaspeake Bay was not influenced by salinity. Instead, resource availability was the principal influence on Macoma balthica. McLusky & Allan (1976) reported that 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.

Streblospio shrubsolii occurred in subtidal areas of the Thames estuary as well as intertidal flats, suggesting the species is resistant to higher salinities than the ‘variable’ levels occurring higher in estuaries (Attrill, 1998). Likewise Tubificoides benedii has been recorded  in high abundance in offshore areas of the North Sea (Gray et al., 1990). Although evidence was limited on response of these species to rapid increases in salinity it is likely they would be resistant to an increase to the fully marine category (30-40 ‰).

Hylleberg (1975) also found that under controlled conditions of salinity ranging from 10 to 30?⁄??and temperatures ranging from 5 to 35° C, Hydrobia ulvae has maximal egestion at the combination of high salinity (30?⁄??) and high temperature (30° C). The species would be likely to show high resistance to an increase in salinity from the reduced and variable conditions the biotope occurs within. 

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 levels.

Oligochaete dominated biotopes are recorded from a range of salinity regimes from full (LS.LSa.MoSa.Ol; LS.LSa.MoSa.Ol.FS), variable (SS.SMu.SMuVS.CapTubi) to low (SS.SMu.SMuVS.LhofTtub) habitats (JNCC,2015). The species characterizing these biotopes are likely to vary. Giere & Pfannkuche (1982) identified how species change over a hypothetical salinity gradient with marine stenohaline species present at full salinities replaced by more euryhaline oligochaete species including Tubificoides benedii and Tubificoides pseudogaster, Paranais litoralis and Baltidrilus costata (formerly Heterochaeta costata).  Studies in the Rhine delta have found that Tubificoides benedii, is more tolerant of a range of salinities than Baltidrilus costata (as Heterochaeta costata) which preferred shallow water brackish stations (Verdonschot et al. 1982). However, numerous studies suggest that Baltidrilus costata tolerates a wide range of salinities from 1‰ to 28‰ (Giere & Pfannkuche, 1982 and references therein), suggesting that while tolerant of some changes, an increase to full salinity may lead to reductions in abundance of this species.

Sensitivity assessment. Hediste diversicolor and other characterizing species are likely to tolerate increased salinity levels above the reduced and variable levels encountered in the biotope and variant sub-biotopes. Biotope resistance is, therefore, assessed as ‘High’ and resilience as ‘High’ (by default) and the biotope is considered to be ‘Not sensitive’. In locations with extremely sheltered conditions and gravelly mud is present where the biotope LS.LMx.GvMu.HedMx.Scr characterized by Hediste diversicolor and Scrobicularia plana occurs it is possible a transition to this variant sub-biotope will occur. However, sediment is more likely to be a stronger factor influencing community structure. 

Salinity decrease (local)

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

Evidence

The sub-biotopes; LS.LMx.GvMu.HedMx.Mac, LS.LMx.GvMu.HedMx.Scr, LS.LMx.GvMu.HedMx.Str, LS.LMx.GvMu.HedMx.Cir, LS.LMx.GvMu.HedMx.Cvol, occur in reduced (18-30 ppt) or variable (18-35 ppt) salinity, whereas LS.LMx.GvMu.HedMx.Scr occurs in full salinity (30-35 ppt) (JNCC, 2015). It is noted that there are relatively few records in each sub-type, leading to uncertainty over the precise nature of the habitat, regarding salinity regime and other factors (JNCC, 2015). As most examples of this biotope occur in reduced or variable salinity the decrease in salinity assessed at the benchmark is to low salinity (<18 ppt). The available evidence (summarised below) suggests that the characterizing species are tolerant of a short-term decrease to low salinity but it is likely that for species such as Macoma balthica long-term reductions would lead to mortality.

The key characterizing species Hediste diversicolor is known to tolerate low salinities below 18-24 psu and it has been shown to replace Arenicola marina in areas influenced by freshwater runoff or input (e.g. the head end of estuaries) (Barnes; 1994; Hayward, 1994). Lower salinities (<8 psu) can, however, have an adverse effect on Hediste diversicolor reproduction (Ozoh & Jones, 1990; Smith 1964). Fertilization in Hediste diversicolor is adapted to high salinity but not to low salinity below 7.63‰ (Ozoh & Jones, 1990). A decrease in salinity at the benchmark pressure (reduction to <18‰ ) may negatively impact recruitment and abundance if the dilution is close to that threshold.

Conde et al. (2013) found that Streblospio shrubsolii were a dominant species in low salinity, estuarine conditions (5-9‰) in the Tagus estuary, Portugal. In Ria de Averio, western Portugal Streblospio shrubsolii and Tubificoides benedii were characterizing species of communities in estuarine sample sites further upstream with lower salinity, suggesting a high resistance to a decrease in salinity (Rodrigues et al., 2011).  Numerous studies suggest that the oligochaete Baltidrilus costata tolerates a wide range of salinities from 1‰ to 28‰ (Giere & Pfannkuche, 1982 and references therein), suggesting that this species is likely to still be present in the biotope.Oligochaete dominated biotopes are recorded from a range of salinity regimes from full (LS.LSa.MoSa.Ol; LS.LSa.MoSa.Ol.FS), variable (SS.SMu.SMuVS.CapTubi) reduced (SS.SMu.SMuVS.CapTubi; LS.LMu.UEst.Tben ) and low (SS.SMu.SMuVS.LhofTtub) habitats (JNCC,2015). In very low salinities from <15 to 0 ‰ species such as Limnodrilus spp. and Tubifex tubifex are found (Giere & Pfannkuche, 1982).  A decrease in salinity at the pressure benchmark would probably result in replacement by oligochaete species more tolerant of lower salinities such as Limnodrilus hoffmeisteri and Tubifex tubifex that characterize the low salinity biotope SS.SMu.SMuVS.LhofTtub.

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 animal’s 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 resistant to  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, quickly return 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.).

Corophium volutator is an exceptionally euryhaline species able to tolerate 2-50 psu (McLusky, 1968) but growth is fastest at 15-20 psu (McLusky, 1970 cited in Meadows & Ruagh, 1981). Corophium volutator is a hyperosmotic regulator and the tolerance of its tissues is 13-50 psu but it needs a salinity of above 5 psu in order to moult, since osmoregulation is lost during moulting (McLusky, 1967). A salinity of at least 7.5 psu is required for reproduction (McLusky, 1968). Changes in salinity may alter population distribution and dynamics as the species is likely to move to more favourable conditions but are very unlikely to cause mortality.

Muus (1967) revealed that Hydrobia ulvae did not crawl into water with a salinity lower than 9?⁄??. Hylleberg (1975) also found that under controlled conditions of salinity ranging from 10 to 30?⁄?? and temperatures ranging from 5 to 35°C, shows that Hydrobia ulvae has maximal egestion at the combination of high salinity (30?⁄??) and high temperature (30° C).

Sensitivity assessment. It is considered likely that a decrease in salinity at the pressure benchmark will lead to some species replacement by polychaetes and oligochaetes more tolerant of low salinity. Hediste diversicolor and oligochaetes are likely to remain but Macoma balthica is likely to reduce in low salinity conditions. A similar biotope could remain where salinities were close to 18 ppt but a severe reduction in salinity would probably lead to loss of the biotope. Resistance is therefore assessed as ‘Low’.  Resilience (following restoration of typical conditions) is ‘High’ and sensitivity is assessed as ‘Low’. It should be noted that resistance would be lower, and sensitivity greater, where salinity was reduced to a level close to freshwater.

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

Hediste diversicolor characteristically inhabits littoral mudflats predominantly of clay (particles < 4 µm), silt (4-63 µm) and to a lesser extent, very fine sand (63-125 µm) (Jones et al., 2000). Highest abundances occur in very weak (negligible) to weak < 1 knot (<0.5 m/sec.) currents. These conditions are provided by this biotope, which occurs in extremely sheltered gravelly mud to gravelly sandy mud on the mid and lower shore.

The type direction and speed of the currents control sediment deposition within an area. Finer sediment will fall to the substratum in weaker currents. An increase in water flow rate would entrain and maintain particles in suspension and erode the mud. As a result the scouring and consequent redistribution of components of the substratum would alter the extent of suitable habitat available to populations of Hediste diversicolor and other species in the biotope that prefer finer sediment. Recovery of Hediste diversicolor would be influenced by the length of time it would take for the potential habitat to return to a suitable state for recolonization by adult and juvenile specimens from adjacent habitats, and the establishment of a breeding population. Recolonization may take between one and three years, as populations differ in reaching maturity (Dales, 1950; Mettam et al., 1982; Olive & Garwood, 1981), from the time that the habitat again becomes suited to the species.

Small Corophium volutator cannot resettle after swimming at current speeds approx. 0.1 m/s (Ford & Paterson, 2001), which probably explains why they mainly swim at high tide (Hughes, 1988). An increase in water flow rate could cause swimming Corophium volutator to be swept away from suitable habitat and cause high mortality. Decreases in flow rate are not considered to negatively impact Corophium volutator.

Coarser sediments are likely to remain in areas of strongest flow velocity (where finer particles have been re-suspended). Species such as Pygospio elegans and other opportunist polychaetes that tolerate coarser particle size will possibly increase in abundance. Macoma balthica is likely to experience greater impact from increased water flow as the species thrives in low energy environments, such as the extremely sheltered areas that characterize the biotope (Tebble, 1976). Increased water flow rate is likely to influence the sediment characteristics in this biotope, primarily by re-suspending and preventing deposition of finer particles (Hiscock, 1983). This is likely to result in erosion of the preferred habitat, which may cause mortality of some portion of the population of Macoma balthica. Higher current velocity (18 cm/s 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) reported that, towards the mouth of an estuary where sediments became coarser and cleaner, Macoma balthica was replaced by another tellin species, Tellina tenuis.

Experimental increases in near-bed current velocity were achieved over intertidal sandflats by placing flumes on the sediment to accelerate water flows (Zuhlke & Reise, 1994). The increased flow led to the erosion of up to 4cm depth of surface sediments.  No significant effect was observed on the abundance of Capitella capitata and numbers of Tubificoides benedii and Tubificoides pseudogaster were unaffected, as they probably avoided suspension by burrowing deeper into sediments. This was demonstrated by the decreased abundance of oligochaetes in the 0-1cm depth layer and increased abundance of oligochaetes deeper in sediments (Zuhlke & Reise, 1994).  A single storm event had a similar result with decreased abundance of oligochaetes in surficial layers, coupled with an increase in deeper sediments (Zuhlke & Reise, 1994). Although Tubificoides spp. can resist short-term disturbances their absence from sediments exposed to higher levels of disturbance indicate that they would be sensitive to longer-term changes in sediment mobility (Zuhlke & Reise, 1994). Birtwell and Arthur (1980) reported seasonal changes in abundance in Baltidrilus costata (as Tubifex costatus) which they attributed to erosion of the upper sediment layers caused by high river flows and wave action.

Sensitivity assessment. Macoma balthica and Corophium volutator abundance may be reduced if juveniles are washed from the substratum and adults are not able to resettle. Loss of mud content in some areas is possible and would lead to replacement by another species but this is unlikely at the pressure benchmark levels. An increase in flow velocity may alter sediments, resistance has been assessed as ‘Medium’, recoverability is assessed as ‘High’ and sensitivity is, therefore ‘Low’.

Emergence regime changes

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

Evidence

The biotope LS.LMx.GvMu.HedMx, occurs from the strandline to the lower shore (JNCC, 2015) and changes in emergence are unlikely to affect the biotope where it remains within an intertidal habitat. The variant sub-biotopes are found on the lower, mid and upper shopre, with the exception of LS.GvMu.Hedmx.St, which is found on the lower and mid shore (JNCC, 2015). 

Hediste diversicolor inhabits a burrow within the sediment which may be up to 0.3 m deep. The species retreats within the burrow during periods of exposure, protecting it from desiccation although increased emergence may cause a decline in the abundance of Hediste diversicolor at the upper limits of the intertidal zone, as they may become stressed by desiccation if the substrata begin to dry and are prone to more extremes of temperature. Hediste diversicolor is sufficiently mobile to gradually retreat back to damper substrata. Gogina et al. (2010) analysed patterns of benthic community distribution related to selected environmental parameters, including depth, in the western Baltic Sea with depths ranging from 0 m to 31 m. Hediste diversicolor displayed a preference for low-saline regions shallower than 18 m. Increased depth had the largest negative effect of all factors influencing distribution and abundance decreased with greater dept) Gogina et al. (2010).

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 intertidally.  Hence, it would be expected to resist 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. Coastal squeeze from sea level rise would produce steeper and more homogenous beach face profiles. Macoma balthica was predicted to be lower on steeper beach faces and biomass of Macoma balthica was predicted to decrease (Fujii & Raffaelli, 2008). 

Tubificoides benedii is capable of penetrating the substratum to depths of 10 cm, shows a resistance to hypoxia and is often typified as an ‘opportunist’ that is adapted to the rapid environmental fluctuations and harsh conditions in estuaries (Gogina et al., 2010). Highest abundances were predicted by  Gogina et al. (2010) to be related to depth with an optimum of 10 m  to 20 m. The evidence  suggests that  abundance may be limited by a decrease in high water level or a change in time (increase) where substratum is not covered by the sea. An increase in the time the biotope is covered by the sea is likely to result in increased abundance of Tubificoides benedii.

Opportunistic, deposit feeding polychaetes, such as the characterizing Pygospio elegans and Streblospio shrubsolii, tolerate stressful conditions, and often out-compete more sensitive species in inter-tidal environments due to greater tolerances. Gogina et al. (2010) indicate that Pygospio elegans favours shallower water, but this modelling study suggested the response against increasing depth is not as rapid as in the case of Hediste diversicolor.

Sensitivity assessment. The biotope and characterizing species are found at a range of shore heights and are considered relatively resistant to changes in emergence which do not alter the extent of the intertidal. An increase in emergence is likely to decrease the upper shore extent of Hediste diversicolor dominated biotopes at the land-ward extent of the intertidal as desiccation increases. A decrease in emergence under the benchmark pressure  is likely to extend the upper extent of the biotope as the species recolonize or migrate to favourable conditions. Biotope resistance is, therefore, assessed as ‘High’, recoverability is assessed as ‘High’ (by default) and the biotope is considered to be 'Not sensitive'.

Wave exposure changes (local)

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

Evidence

This biotope occurs in wave sheltered areas, where estimated wave categories range from sheltered, very sheltered and extremely sheltered (JNCC, 2015). The key characterizing species Hediste diversicolor is infaunal, inhabiting a burrow in which it seeks refuge from predators and may partially emerge to seek and capture food. An alteration of factors within the environment that increases wave exposure could cause erosion of the substrata and consequently, loss of habitat.

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), limiting food availability, however impacts from this pressure at the benchmark levels may be low for this biotope, as the biotope is limited to sheltered or extremely 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. Where less sheltered conditions occur the sub biotope LS.LMx.GvMu.HedMx.Mac is likely to dominate as this variant occurs in the least sheltered conditions.

Sensitivity assessment. Resistance to a change in nearshore significant wave height >3% but <5% of the two main characterizing species Hediste diversicolor 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 ‘High’ resistance through their traits to live relatively deep in the sediment. Resilience (recoverability) is also ‘High’ giving a Sensitivity of ‘Not Sensitive’. 

Transition elements & organo-metal contamination

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

Evidence

This pressure is Not assessed but evidence is presented where available. The following review discusses impacts at higher concentrations than the pressure benchmark.

In Hediste diversicolor the acute toxicity is dependent on the rate of uptake of the metal, since this determines the speed with which the lethal dose is built up. The rate of intake is important because this determines whether the organism's detoxification mechanisms can regulate internal concentrations. The resistance of Hediste diversicolor is thought to be dependent on a complexing system which detoxifies the metal and stores it in the epidermis and nephridia (Bryan & Hummerstone, 1971; McLusky et al. 1986).

Hediste diversicolor has been found successfully living in estuarine sediments contaminated with copper ranging from 20 µm Cu/g in low copper areas to >4000 µm Cu/g where mining pollution is encountered e.g. Restronguet Creek, Fal Estuary, Cornwall (Bryan & Hummerstone, 1971). Attempts to change the tolerance of different populations of Hediste diversicolor to different sediment concentrations of copper have shown that it is not readily achieved suggesting that increased tolerance to copper has a genetic basis (Bryan & Hummerstone, 1971; Bryan & Gibbs, 1983).

Crompton (1997) reviewed the toxic effect concentrations of metals to marine invertebrates Annelid species, such as Hediste diversicolor were found to be at risk if metals exceeded the following concentrations during 4-14 days of exposure: >0.1 mg Hg l^-1, > 0.01 mg Cu l^-1, > 1 mg Cd l^-1, >1 mg Zn l^-1,>0.1 mg Pb l^-1, >1 mg Cr L^-1, >1 mg As l^-1 and >10 mg Ni l^-1. In general, for estuarine animals heavy metal toxicity increases as salinity decreases and temperature increases (McLusky et al., 1986). For example, Fernandez & Jones (1990) calculated 96 hour LC₅₀ Zinc values for Hediste diversicolor at four salinities 5, 10, 17.5 and 30 psu at 12°C. The 96 hour LC₅₀ at 17.5 psu and 12°C was 38 mg Zn l^-1, while at 5 and 10 psu it was 7 and 19 mg Zn l^-1 respectively. Toxicity decreased with increasing salinity. When salinity remained constant at 17.5 psu, but temperature varied, the following 96 hour LC ₅₀ values for Zinc were recorded: 40 mg Zn l^-1 at 6°C, 32 mg Zn l^-1 at 12°C and 9.1mg Zn l^-1 at 20°C. Toxicity increased with increasing temperature. Accumulation of zinc was also greater at the lowest salinities and when the temperature was highest at 20°C. In a parallel experiment, the presence of sediment was found to reduce toxicity and body accumulation of zinc in Hediste diversicolor. Recovery of this species would be influenced by the length of time it would take for the potential habitat to return to a suitable state (e.g. factors such as the decline of bioavailable metals within the marine environment), recolonization by adult and juvenile specimens from adjacent habitats, and the establishment of a breeding population. Since juveniles remain in the infauna throughout their development selection for metal tolerance can be expected to be operative from an early stage (Bryan & Gibbs, 1983).

Corophium volutator is highly intolerant of metal pollution at levels often found in estuaries from industrial outfalls and contaminated sewage. A concentration of 38 mg Cu/l was needed to kill 50% of Corophium volutator in 96 hour exposures (Bat et al., 1998). Other metals are far more toxic to Corophium volutator, e.g. zinc is toxic over 1 mg/l and toxicity to metals increases with increasing temperature and salinity (Bryant et al., 1985). Mortality of 50% is caused by 14 mg/l (Bat et al., 1998). Although exposure to zinc may not be lethal, it may affect the perpetuation of a population by reducing growth and reproductive fitness. Mercury was found to be very toxic to Corophium volutator, e.g. concentrations as low as 0.1 mg/l caused 50% mortality in 12 days. Other metals known to be toxic include cadmium, which causes 50% mortality at 12 mg/l (Bat et al., 1998), and arsenic, nickel and chromium which are all toxic over 2 mg/l (Bryant et al., 1984; Bryant et al., 1985a; 1985).

Scrobicularia plana can detect copper at a concentration of 0·01 ppm. The initial response is valve closure resulting in a rapid drop in heart rate. In concentrations of 0·05, 0·01 and, to a lesser extent, 0·1 ppm copper added to seawater, the clams begin to interact with the polluted water after 2–3 h. In 0·5 ppm, the valves remain closed and the heart rate is maintained at a low level over the 6-h exposure period. Mortality increases with time in 0·5 ppm copper concentration, reaching 50% in 5–7 days. In 0·05 and 0·01 ppm, no mortality was recorded over this period (Akberali & Black, 1980).Two experimental 30 day long static toxicity tests on small spat (2 to 3 mm in length) of Scrobicularia plana were undertaken on the effects of copper on the survival and burying activity in sand, of juveniles. Results showed that:

1) exposure to up to 80 µg Cu 1.' did not result in increased mortalities with respect to the controls;

2) Cu concentrations at 20 µg l^-1and above also increased the burying time of juveniles by the end of the experiment; and

3) the no-observed-effect concentration (NOEC) for Cu was the lowest dose tested (i.e. 10 µg I-'). (Ruiz et al., 1994).

Alterations of the burrowing behaviour of Scrobicularia plana, were studied in individuals exposed to soluble copper. Animals were exposed for 4 d to concentrations ranging from 25 to 150 μ g Cu l− 1. At the end of exposure, the burrowing kinetics in clean sediment were determined after 1 and 2 days. Even at the lowest tested concentrations, copper caused hypoactivity in organisms belonging to both species studied. Metabolical or physiological disturbances could be the cause of these impairments. Concentrations affecting burrowing behaviour were below those responsible for mortality in these species (Bonnard et al., 2009).

Laboratory tests in clean water can be misleading as these do not reflect lowered toxicity in the marine environment due to the buffering effects of carbon and sulphide which render copper non-labile (not bioavailable) and the influence of water pH, hardness, temperature and salinity etc. Field surveys have found that Scrobicularia plana is present in the highly contaminated Fal Estuary where levels of copper and zinc are high (Bryan & Gibbs, 1983).

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

Rygg (1985) classified Tubificoides spp as highly tolerant species, common at the most copper polluted stations (>200 mg Kg-1) in Norwegian fjords.

Hydrocarbon & PAH contamination

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

Evidence

This pressure is Not assessed but evidence is presented where available. The following review discusses impacts at higher concentrations than the pressure benchmark.

The 1969 West Falmouth (America) spill of Grade 2 diesel fuel documents the effects of hydrocarbons in a sheltered habitat (Suchanek, 1993). The entire benthic fauna including Hediste diversicolor was eradicated immediately following the spill and remobilization of oil that continued for a period > 1 year after the spill, contributed to much greater impact upon the habitat than that caused by the initial spill. Effects are likely to be prolonged as hydrocarbons incorporated within the sediment by bioturbation will remain for a long time owing to slow degradation under anoxic conditions. Oil covering the surface and within the sediment will prevent oxygen transport to the infauna and promote anoxia as the infauna utilize oxygen during respiration. Although Hediste diversicolor is tolerant of hypoxia and periods of anoxia, a prolonged absence of oxygen will result in the death of it and other infauna. McLusky (1982) found that petrochemical effluents released from a point source to an estuarine intertidal mudflat, caused severe pollution in the immediate vicinity. Beyond 500 m distance the effluent contributed to an enrichment of the fauna in terms of abundance and biomass similar to that reported by Pearson & Rosenberg (1978) for organic pollution, and Hediste diversicolor was found amongst an impoverished fauna at 250 m from the discharge.

Analysis of Scrobicularia plana collected in April 2008 from three estuaries along a pollution gradient (Goyen < Loire < Seine) found sub-lethal effects on clams including neurotoxicity and impairment of digestive enzyme activities (cellulase or amylase) in the Loire and Seine estuaries. The highest lactate dehydrogenase activity was registered in the Loire estuary, in parallel with enhanced levels of vanadium (a metal present in petroleum), likely as a consequence of a small oil spill that occurred one month before the sampling collection. The median size was significantly lower in clams exposed to direct (chemicals) or indirect (available food) effects in the most contaminated site. Burrowing behaviour was disturbed in clams from both of the Loire and Seine estuaries, a response probably due to physiological impairment rather than to avoidance of contaminated sediment. The activation of defence mechanisms towards metals (metallothionein) and other classes of contaminants (the biotransformation enzyme glutathione-S-transferase) do not ensure a total protection since a number of impairments were observed at the infra-organismal (AChE and digestive enzyme activities) and individual (burrowing behaviour) levels in relation to the degree of anthropogenic pressure. However, even in the most contaminated estuary (Seine), historical records do not show a consistent decrease of Scrobicularia plana populations (cited from Boldina-Cosqueric et al., 2010).

Light fractions (C10 - C19) of oils are much more toxic to Corophium volutator than heavier fractions (C19 - C40). In exposures of up to 14 days, light fraction concentrations of 0.1 g/kg sediment caused high mortality. It took 9 g/kg sediment to achieve similar mortalities with the heavy fraction (Brils et al., 2002). In the Forth Estuary, Corophium volutator was excluded for several hundred metres around the outfalls from hydrocarbon processing plants. Roddie et al. (1994) found high levels of mortality of Corophium at sites contaminated with crude oil.

In Finland in oligohaline inland waters near an oil refinery, Baltidrilus costata (as Tubifex costatus) appeared to be sensitive to oil pollution and had completely disappeared from sediments exposed to pollution and did not recolonize during a 4year post pollution period (Leppäkoski & Lindström, 1978). Tubificoides benedii appears to be more tolerant and was found in UK waters near oil refineries as the sole surviving member of the macrofauna. Populations were however apparently reduced and the worms were absent from areas of oil discharge and other studies indicate sensitivity to oiling (Giere & Pfannkuche, 1982, references therein).

Synthetic compound contamination

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

Evidence

This pressure is Not assessed but evidence is presented where available. The following review discusses impacts at higher concentrations than the pressure benchmark.

Reports of the effects of synthetic chemicals on Hediste diversicolor illustrate that the intolerance of the species is highly dependent upon the molecular structure of the chemical, which determines the chemicals properties and use. For example:

1. Collier & Pinn (1998) observed significant differences in both the abundance and biomass of a benthic community from the Ythan Estuary, Scotland, experiencing contamination by Ivermectin. Ivermectin is the 22,23-dihydro derivative of avermectin ß which has been shown to be highly efficient in the treatment of sea lice. Hediste diversicolor was the most intolerant species to Ivermectin in the benthic community studied. A rapid decline in both abundance and total biomass of Hediste diversicolor occurred within 7 days and with increasing concentration. An Ivermectin concentration of 8.0 mg m² caused 100% mortality within 14 days. Davies et al., (1998) modelled factors influencing the concentration of Ivermectin reaching the seabed which ranged from 2.2 to 6.6 mg m². The upper limit of this range was only slightly less than the concentrations found to be toxic by Collier & Pinn (1998) and Black et al. (1997). Davies et al.(1998) concluded that there was a significant risk to benthic organisms within a radius of 50 m of salmon farms utilizing Ivermectin and that Ivermectin could accumulate (half life of Ivermectin in marine sediments > 100 days) within the sediment beyond a single treatment and reach toxic levels.
2. In contrast, Craig & Caunter (1990) examined the effects of the organosilicon compound, Polydimethylsiloxane (PDMS) in sediment on Hediste diversicolor. PDMS fluids are less dense than water and insoluble and form a discrete layer on the surface of the water. In an intertidal environment PDMS fluids are deposited upon the sediment surface at low tide and into contact with Hediste diversicolor. In laboratory tests, exposure to 10,000 mg PDMS per kg of sediment caused no deaths over 96 hours, and exposure to 1,000 mg PDMS per kg of sediment caused no deaths of Hediste diversicolor after 28 days.

Recovery of this species would be influenced by the length of time it would take for the potential habitat to return to a suitable state (e.g. factors such as the rate of decay of the synthetic chemical within the marine environment), recolonization by adult and juvenile specimens from adjacent habitats, and the establishment of a breeding population. This may take between one and three years, as populations differ in reaching maturity (Dales, 1950; Mettam et al., 1982; Olive & Garwood, 1981), from the time that the habitat again becomes suited to the species.

Corophium volutator is paralysed by pyrethrum based insecticide sprayed onto the surface of the mud (Gerdol & Hughes, 1993) and pyrethrum would probably cause significant mortalities if it found its way into estuaries from agricultural runoff. Nonylphenol is an anthropogenic pollutant that regularly occurs in water bodies. It is an oestrogen mimic that is produced during the sewage treatment of non-ionic surfactants and can affect Corophium volutator (Brown et al., 1999). Nonylphenol is a hydrophobic molecule and often becomes attached to sediment in water bodies. This will make nonylphenol available for ingestion by Corophium volutator in estuaries where much of the riverine water-borne sediment flocculates and precipitates out of suspension to form mudflats. Nonylphenol is not lethal to Corophium volutator but does reduce growth and has the effect of causing the secondary antennae of males to become enlarged which can make the amphipods more vulnerable to predators (Brown et al., 1999). Corophium volutator is killed by 1% ethanol if exposed for 24 hours or more, but can withstand higher concentrations in short pulses. Such short pulses, however, have the effect of re-phasing the diel rhythm and will delay the timing of swimming activity for the duration of the ethanol pulse (Harris & Morgan, 1984b).

Radionuclide contamination

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

Evidence

Beasley & Fowler (1976) and Germain et al., (1984) examined the accumulation and transfers of radionuclides in Hediste diversicolor from sediments contaminated with americium and plutonium derived from nuclear weapons testing and the release of liquid effluent from a nuclear processing plant. Both concluded that the uptake of radionuclides by Hediste diversicolor was small. Beasley & Fowler (1976) found that Hediste diversicolor accumulated only 0.05% of the concentration of radionuclides found in the sediment. Both also considered that the predominant contamination pathway for Hediste diversicolor was from the interstitial water. However, there is insufficient information available on the biological effects of radionuclides to comment further upon the intolerance of this species to radionuclide contamination.

Hutchins et al. (1998) described the effect of temperature on bioaccumulation by Macoma balthica of radioactive americium, caesium and cobalt, but made no comment on the intolerance of the species.

Corophium volutator readily absorbs radionuclides such as americium and plutonium from water and contaminated sediments (Miramand et al., 1982). However, the effect of contamination of the individuals was not known but accumulation through the food chain was assumed (Miramand et al., 1982).

Further, direct assessments of impacts at the benchmark pressure on benthic communities, and this biotope in particular were not found.

Sensitivity assessment. No evidence. Insufficient evidence was available to complete and assessment.

Introduction of other substances

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

Evidence

This pressure is Not assessed.

De-oxygenation

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

Evidence

The habitats which Hediste diversicolor inhabits tend to have lower oxygen levels than other sediments. Hediste diversicolor is resistant to moderate hypoxia (Diaz & Rosenberg, 1995). Vismann (1990) demonstrated a mortality of only 15% during a 22 day exposure of Hediste diversicolor at 10% oxygen (ca. 2.8 mg O₂ per litre). Hediste diversicolor is active at the sediment/water interface where hydrogen sulphide concentrations increase during periods of hypoxia. Vismann (1990) also demonstrated that the high tolerance of Hediste diversicolor to hypoxia in the presence of sulphide is enabled by elevated sulphide oxidation activity in the blood. Hediste diversicolor may also exhibit a behavioural response to hypoxia by leaving the sediment (Vismann, 1990) in the presence of sulphide. After 10 days of hypoxia (10% oxygen saturation) with sulphide (172-187 µmM) only 35% of Hediste diversicolor had left the sediment compared to 100% of Nereis virens. Laboratory experiments in the absence of sediments, found that Hediste diversicolor could survive hypoxia for more than 5 days and that it had a higher tolerance to hypoxia than Nereis virens, Nereis succinea and Nereis pelagica (Theede, 1973; Dries & Theede, 1974; Theede et al., 1973). Juvenile Hediste diversicolor survived hypoxic conditions for 4 days in laboratory conditions and combined hypoxia and increased sulphide (1 mmo1 1-') for 3 days (Gamenick et al., 1996). Post larvae Hediste diversicolor were the only life stage to show les tolerance to hypoxia, surviving for only 14 hr (Gamenick et al., 1996).

Macoma balthica appears to be relatively tolerant of de-oxygenation. Brafield & Newell (1961) frequently observed that, in conditions of oxygen deficiency (e.g. less than 1 mg O₂/l), Macoma balthica  displayed survivability of low oxygen concentrations and shell growth continued (Jansson et al., 2015). Although, sub-lethal effects of hypoxia have been identified as 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 Macoma balthica to resist extreme oxygen deficiency was mainly due to anaerobic metabolism. 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.

The characterizing oligochaetes and polychaetes within the biotope that display tolerance to hypoxia include Tubificoides benedii and Capitella capitata, while Pygospio elegans is highly sensitive to hypoxia (Gogina et al., 2010). Exposure to dissolved oxygen concentration of less than or equal to 2 mg/l for 1 week is likely to limit Pygospio elegans abundance, whilst having limited impact on Tubificoides benedii and Capitella capitata populations.

Corophium volutator is highly sensitive to hypoxia and suffers 50% mortality after just 4 hours in hypoxic conditions, or in 2 hours if there is rapid build-up of sulphide (Gamenick et al., 1996). These conditions often occur in estuaries where drifting macroalgae (such as Fucus sp.) settle on the mudflats in small patches.

Oligochaete species vary in their tolerance of hypoxia and associated high sulphide levels. Most enchytraeids and naidids are sensitive to hydrogen sulphide and hypoxia while tubificids are often more resistant (Giere, 2006).

Tubificoides benedii has a high capacity to tolerate anoxic conditions, its extreme oxygen tolerance  is based on an unusually low respiration rate (Giere et al., 1999).  Respiration rates of Tubificoides benedii measured at various oxygen concentrations showed that aerobic respiration is maintained even at very low oxygen concentrations (Giere et al., 1999). Birtwell & Arthur (1980) showed that Tubificoides benedii could tolerate anoxia in the Thames Estuary (LT₅₀ = 58.8 hours at 20^oC, 26.6 hours at 25^oC  and 17.8 hours at 30^oC in experiments with worms acclimated to 20^oC.)

Tolerance experiments by Gamenick et al.  (1996) found that Baltidrilus costata  (as Heterochaeta costata) was not affected by hypoxic conditions for at least 3 days but the addition of sulphide 91.96 mmol/litre) caused mortality after 1 day (Gamenick et al., 1996).

Sensitivity assessment. Resistance to exposure to dissolved oxygen concentration of less than or equal to 2 mg/l for 1 week is assessed as ‘High’ for the characterizing species Hediste diversicolor and Macoma balthica. It is important to consider that other species that are common or abundant in the biotope may be impacted by decreased dissolved oxygen, such as Pygospio elegans and decreases in abundance of these species are likely. As this biotope is found in intertidal habitats oxygen levels will be recharged during the tidal cycle lowering exposure to this pressure for Pygospio elegans. Based on the reported tolerances for anoxia and intertidal habitat, biotope resistance is assessed as ‘High’ resilience is assessed as ‘High’ (by default) and the biotope is considered to be ‘Not sensitive’ at the benchmark level

Nutrient enrichment

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

Evidence

This pressure relates to increased levels of nitrogen, phosphorus and silicon in the marine environment compared to background concentrations.  The benchmark is set at compliance with WFD criteria for good status, based on nitrogen concentration (UKTAG, 2014).  Primary production in the biotope will be limited to microalagae at the sediment surface, rather than macroalgae. Changes in primary production as a result of changes in nutrient enrichment are, therefore, not considered likely to directly alter the biotope.

Aberson et al. (2016) found nutrient enrichment promotes surface deposit feeding in Hediste diversicolor, over suspension feeding and predation. At sewage-polluted sites in three estuaries in  SE  England Hediste diversicolor mainly consumed microphytobenthos, sediment organic matter and filamentous macroalgae Ulva  spp. At cleaner  sites  Hediste diversicolor relied more on suspension feeding and consumption of Spartina anglica (Aberson et al., 2016). Whilst suggesting adaptability to nutrient enrichment this behaviour will increase predation risk.

Nutrient enrichment favours the growth of opportunistic green macro-algae blooms which can cause declines in some species and increases in others (Raffaelli, 2000). Evidence (Beukema, 1989; Reise et al., 1989; Jensen, 1992) suggested a doubling in the abundance of Hediste diversicolor in the Dutch Wadden Sea, accompanied by a more frequent occurrence of algal blooms that were attributed to marine eutrophication. Algae may be utilized by Hediste diversicolor in its omnivorous diet, so some effects of nutrient enrichment may be beneficial to this species. However, evidence for the effects of algal blooms stimulated by nutrient enrichment on Hediste diversicolor is not consistent. Raffaelli (1999) examined a 30 year data base to examine the effect of nutrient enrichment on an estuarine food web in Aberdeenshire, Scotland. This study displayed impacts to species characterizing the biotope from development of algal mats, the density and distribution of which was related to nutrient. In areas where algal biomass was greatest reduced invertebrate densities were recorded. The mud shrimp Corophium volutator showed the greatest decrease in density. Densities of Corophium volutator, Macoma balthica and Hediste diversicolor were lower in 1990 compared to 1964 at sites where macro-algal mats increased over the same period. Conversely, densities were on average higher in the upper reaches where macroalgal mats were generally absent before 1990 (Raffaelli, 1999). Capitella capitata and Pygospio elegans abundance were greater in areas that received greatest nutrient enrichment (Raffaelli, 1999). Long-term nutrient enrichment may, therefore, alter the biotope if high biomass of algal mats persists.

In the Ythan Estuary, Scotland, nutrient enrichment causes the mudflats to become covered with algal mats consisting mainly of the gutweed Ulva intestinalis. These mats physically perturb Corophium volutator by preventing burrowing and normal feeding. In areas where the mats did not occur, the density of Corophium volutator was 11 times higher than under the algae. When the algae died back in the winter, the areas were rapidly recolonized by Corophium volutator from adjacent patches where the gutweed could not grow and population growth was high from feeding on the rotting algae. In the spring, the gutweed returned and the Corophium volutator were excluded once again (Raffaelli et al., 1991).

Sensitivity assessment.  The benchmark is relatively protective and is not set at a level that would allow blooms of green algae on the sediment, based on this consideration and based on the lack of primary producers structuring the biotope, resistance is assessed as 'High' and resilience as 'High' (by default), so that the biotope is assessed as 'Not sensitive'.

Organic enrichment

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

Evidence

All species apart from two that are abundant in the biotope are classed in a Marine Biotic Index as being indifferent to, tolerating or proliferating under organic enrichment conditions (Borja et al., 2000). Only Macoma balthica and Manayunkia aestuarina are recorded as being sensitive to organic enrichment. However, case studies display resilience of Macoma balthica populations to enrichment. Macoma balthica have been shown experimentally to be able 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 in the 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). Tubificoides benedii  and other oligochaetes are very tolerant of high levels of organic enrichment and often dominate sediments where sewage has been discharged or other forms of organic enrichment have occurred (Pearson & Rosenberg, 1978; Gray, 1971; McLusky et al., 1980). 

Borja et al. (2000) and Gittenberger & Van Loon (2011) both assigned Corophium volutator to Group III ‘Species tolerant to excess organic matter enrichment; these species may occur under normal conditions, but their populations are stimulated by organic enrichment (slight unbalance situations).

In Ria de Averio, western Portugal Streblospio shrubsolii and Tubificoides benedii were characterizing species of communities further upstream in estuarine sample sites, at sites with increased organic matter (Rodrigues et al., 2011). Streblospio shrubsolii are also considered characteristic species communities in polluted environments, suggesting the species is likely to be resistant to increased organic enrichment (Cooksey & Hyland, 2007).

Tubificoides benedii and Baltidrilus costatus are both very tolerant of high levels of organic enrichment and often dominate sediments where sewage has been discharged or other forms of organic enrichment have occurred (Pearson & Rosenberg, 1978; Gray, 1971; McLusky et al., 1980). Their tolerance for organic enrichment is attributed to their adaptation to live in and feed on enriched organic deposits (Pearson & Rosenberg, 1978) and their high population densities in such areas is enhanced by the lack of predation and competition. Tubificoides benedii are abundant in mussel beds (mussel relaying may be the source of smothering) which  has been attributed to their tolerance of organically rich deoxygenated sediment (Commito & Boncavage, 1989). Tubificoides benedii has also been found in elevated abundances in areas of organic enrichment around fish farms (Haskoning, 2006).

Sensitivity assessment. At the benchmark levels, a resistance of ‘High’ as the main characterizing species Hediste diversicolor is tolerant of organic enrichment and an input at the pressure benchmark is considered unlikely to lead to gross pollution effects . A resilience of ‘High’ is assigned (by default) and the biotope is assessed as ‘Not sensitive’.

Physical loss (to land or freshwater habitat)

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

Evidence

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

Physical change (to another seabed type)

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

Evidence

This biotope and sub-biotopes is only found in sediment, in particular, gravelly sandy mud or gravelly mud (JNCC, 2015). The burrowing organisms characterizing this biotope, including Hediste diversicolor, 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. Biotope resistance is assessed as ‘None’, resilience is ‘Very low’ (as the change at the pressure benchmark is permanent) and biotope sensitivity is ‘High’.

Physical change (to another sediment type)

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

Evidence

The benchmark for this pressure refers to a change in one Folk class.  The pressure benchmark originally developed by Tillin et al. (2010) used the modified Folk triangle developed by Long (2006) which simplified sediment types into four categories: mud and sandy mud, sand and muddy sand, mixed sediments and coarse sediments.  The change referred to is, therefore, a change in sediment classification rather than a change in the finer-scale original Folk categories (Folk, 1954).  At the pressure benchmark a change in sediment to sandy mud and muddy sand and muds and increased coarse sediment content (to gravels or sands) is considered. The biotope occurs in gravelly sandy mud and the variant sub biotopes show some variation in species communities and sediment type (JNCC, 2015) so changes in proportion of finer or coarser sediments may lead to some biotope reversions between the sub-biotopes.

1. Decrease of gravel content is likely to lead to change to comparable mud dominated biotopes. Where LS.LMx.GvMu.HedMx occurs it is commonly found with patches of mud and there are broad transition areas between the sub-biotopes of HedMx, and the corresponding muddy sediment biotopes (LS.LMu.UEst.Hed Hediste diversicolor in littoral mud or LS.LMu.MEst.HedMac, Hediste diversicolor and Macoma balthica in littoral sandy mud). A change to finer sediemnts is therefore likely to lead to biotope reclassification but some of the key characterizing species, including Hediste diversicolor  may remain. 
2. An increase in gravel and a change to clean sands or coarse sediments is likely to have a more significant effect as sediment cohesion and ability to retain organic matter and water is reduced altering habitat suitability for burrowing polychaetes and amphipods and deposit feeders.

Hediste diversicolor is infaunal and is reliant upon a muddy/sandy sediment in which to burrow.  Hediste diversicolor has been identified in other intertidal sediments including gravels, clays and even turf (Clay, 1967; Scaps, 2002), although abundance may be reduced in these habitats. 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 a permanent increase in  gravel content. Conde et al. (2011) compared recruitment of Scrobicularia plana to excavated and un-excavated control plots (expected to enhance the deposition of bivalve spat if the settlement of bivalves was the result of a passive process) at different shore levels in Portugal. Juveniles were found to avoid excavated plots, showing significantly higher abundance in control plots. The data strongly suggested that recruited bivalves actively avoid unsuitable substrata, including an increased gravel fraction.

Pygospio elegans can tolerate increased gravel content and has been viewed asan  opportunistic species that is capable of exploiting changes to coarser sediments (Gray, 1981). Therefore, Pygospio elegans are likely to be less affected and even increase in abundance under a change in Folk class to gravelly mud (or a change from sandy mud to muddy sand, or gravelly muddy sand).

Silva et al. (2006) found Streblospio shrubsolii in an estuarine site in western Portugal, were more closely associated with increasing mud content and decreasing gravel content.

Oligochaete dominated biotopes occur in a range of sedimentary habitats, where variable or reduced salinity prevent a more species-rich assemblage developing. Although the lack of identification to species level has hampered understanding of species preferences (and the species that typically occur in this biotope) it is clear that at least some species exhibit strong preferences for sediment type. Tubificoides heterochaetusfor example, sampled in South Carolina salt marsh and tidal inlets was found in significantly greater abundances in coarser sediments where silt and clay fractions were lower (Gillett et al., 2007).

Sensitivity assessment. An increase in mud content is likely to lead to a change to comparable mud dominated biotopes. Case studies display decreasing abundance with increased gravel content of Hediste diversicolor and reduced growth rates of Macoma balthica. Abundance of polychaetes is likely to depend on each species tolerance of increasing gravel content, with species, such as Pygospio elegans, that can exploit the conditions increasing in abundance ) but other species decreasing in abundance. Resistance to a change in one Folk class is assessed as ‘Low’ as changes in sediment will alter the biotope character although some characterizing species may remain. Resilience is assessed as ‘Very Low’ as a change at the benchmark is permanent. The sensitivity of the biotope overall is, therefore, considered to be ‘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 gravelly sandy mud or gravelly mud (Conner et al., 2004).  The characterizing infaunal species, including 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 in the impact footprint and the sediment habitat.

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 (see penetration and disturbance pressure).  At the pressure benchmark the exposed sediments are considered to be suitable for recolonization almost immediately following extraction.  Recovery will be mediated by the scale of the disturbance and the suitability of the sedimentary habitat, biotope resilience is assessed as 'High' (based on recolonization by adults and pelagic larvae) and biotope sensitivity is assessed 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

Muddy sand sediments, in general, tend to be cohesive although high levels of water content will reduce this and destabilise sediments. Sediment cohesion provides some sediment stabilisation to resist erosion following surface disturbance. The characterizing species associated with this biotope are infaunal and hence have some protection against surface disturbance, although siphons of bivalves and tubes of the sedentary polychaete Pygospio elegans, may project above the sediment surface. Damage to tubes and siphons would require repair. The snail Hydroia ulvae is present on the surface and abrasion may result in burial or damage to this species. 

Surface compaction can collapse burrows and reduce the pore space between particles, decreasing penetrability and reducing stability and oxygen content (Sheehan, 2007).  Trampling (3 times a week for 1 month) associated with bait digging reduced the abundance and diversity of infauna (Sheehan, 2007; intertidal muds and sands). The bivalve Scrobicularia plana has a hard shell and can retreat into a long, protective tube, providing some protection from abrasion. Trampling experiments used to assess the impacts of crab-tiling have shown an increase in Scrobicularia plana in trampled plots, indicating that this species has some resistance to this pressure (Sheehan et al., 2010). 

The burrowing life habits of Corophium volutator are likely to provide some protection from abrasion at the surface only. However, any abrasion or physical disturbance is likely to reduce the density of Corophium volutator through emigration and increased mortality. For example, the sediment turnover caused by cockles and lugworms disturbed the burrows of Corophium volutator and caused a significant negative effect on Corophium volutator density as a result of increased rate of swimming making the amphipod more vulnerable to predation (Flach & De Bruin, 1993, 1994).

Experimental studies on crab-tiling impacts have found that densities of Tubificoides benedii and Tubificoides pseudogaster were higher in non-trampled plots (Sheehan et al. 2010), indicating that these oligochaetes have some sensitivity to trampling. Whomersley et al., (2010) conducted experimental raking on intertidal mudflats at two sites (Creeksea- Crouch estuary England and Blackness- lower Forth estuary, Scotland), where Tubificoides benedii were dominant species. For each treatment 1 m² plots were raked twice to a depth of 4cm (using a garden rake). Plots were subject to either low intensity treatments (raking every four weeks) or high (raking every two weeks). The experiment was carried out for 10 months at Creeksea and a year at Blackness. The high and low raking treatments appeared to have little effect on Tubificoides benedii (Whomersley et al., 2010).

Sensitivity assessment. Resistance is assessed as ‘Medium', as abrasion is unlikely to affect high numbers of infaunal burrowing species such as the key characterizing species  Hediste diversicolor and the oligochaetes, but bivalves, tube dwelling polychaetes and Hydrobia ulvae may be reduced in abundance. Resilience is assessed as 'High' and biotope sensitivity is assessed as 'Low'.

Penetration or disturbance of the substratum subsurface

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

Evidence

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 only (see abrasion pressure). A number of studies have assessed the impacts of activities resulting in penetration and disturbance of sediments on the characterizing species in similar habitats. The characterizing species have some protective traits such as infaunal life habit, with deeper burrowing species less exposed. The shells of Scrobicularia plana and Macoma balthica provide some protection. Pygospio elegans inhabits fragile tubes at the sediment surface and Hydrobia ulvae crawl on the sediment, both species are likely to be vulnerable to penetration and disturbance of the sediment.

Ferns et al. (2000) studied effects of harvesting of cockles and reported a decline in muddy sands of 83% in Pygospio elegans (initial density 1850 /m²) when a mechanical tractor towed harvester was used in a cockle fishery. Pygospio elegans and Hydrobia ulvae were significantly depleted for >100 days after harvesting (the limit of the study monitoring timeline).

The effects of  pipeline construction on benthic invertebrates were also investigated using a Before/After impact protocol at Clonakilty Bay, West Cork, Ireland. Benthic invertebrates were sampled once before the excavation and at one, two, three and six months after the completion of the work. Invertebrate samples were dominated by Hediste diversicolor, Scrobicularia plana and Tubifex spp. An impact was obvious in the construction site in that no live invertebrates were found at one month after disturbance, but there followed a gradual recolonisation by Hediste diversicolor. At six months after the disturbance there was no significant difference in the mean number of total individuals (of all species) per core sample amongst all study sites, but the apparent recovery in the impacted area was due to two taxa only, Hediste diversicolor and Tubifex spp. (Lewis et al., 2002).

Corophium volutator burrows to 5 cm deep and is also likely to be removed. However, in the Columbia river, no significant difference was found in Corophium volutator densities before and after dredging a channel and no difference between the dredged site and a control site (McCabe et al., 1998). Presumably, the dredging did cause mortality of Corophium volutator but recolonization was so rapid that no difference was found.

Tubificoides benedii can be relatively deeply buried and could avoid direct exposure to penetration and disturbance of upper sediment layers although sediment disturbance and compaction could damage these soft-bodied species and oligochaetes in general are not found in high abundances in sediments with high levels of disturbance from wave action. Whomersley et al., (2010) conducted experimental raking on intertidal mudflats at two sites (Creeksea- Crouch estuary England and Blackness- lower Forth estuary, Scotland), where Tubificoides benedii were dominant species. For each treatment 1 m² plots were raked twice to a depth of 4cm (using a garden rake). Plots were subject to either low intensity treatments (raking every four weeks) or high (raking every two weeks). The experiment was carried out for 10 months at Creeksea and a year at Blackness. The high and low raking treatments appeared to have little effect on Tubificoides benedii (Whomersley et al., 2010). These results are supported by observations that two experimental passes of an oyster dredge that removed the sediment to a depth of between 15-20 cm did not significantly affect Tubifcoides benedii (EMU, 1992).

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 ‘High’, and sensitivity is assessed as ‘Low’.

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 Hediste diversicolor 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 the characterizing species.

Hediste diversicolor characteristically inhabits estuaries where turbidity is typically higher than other coastal waters. Changes in the turbidity may influence the abundance of phytoplankton available as a food source that may be attained through filter feeding. Hediste diversicolor utilizes various other feeding mechanisms and, at the benchmark level, the likely effects of a change in one rank on the WFD scale are limited.

Corophium volutator lives in areas with very high sediment loads, suggesting an increase in suspended solids would not affect them.

Scrobicularia plana does not require light and therefore would not be affected by a decrease in turbidity for light attenuation purposes. It is possible that decreased turbidity would increase primary production in the water column and by micro-phyto benthos. The resultant increase in food availability may enhance growth and reproduction in this species, but only if food was previously limiting.

Sensitivity assessment. The following sensitivity assessment relies on expert judgement, utilising evidence of species traits and distribution and therefore confidence has been assessed as low. Resistance is ‘High’ as no significant negative effects are identified and potential benefits from increased food resources may occur. 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 degree to which the characterizing species are able to resist this pressure depends primarily on species mobility, ability to survive within sediment without contact with the surface and ability to escape from the over-burden. Factors that affect the ability to regain the surface include grain size (Maurer et al., 1986), temperature and water content (Chandrasekara & Frid, 1998).

Mobile polychaetes have been demonstrated to burrow through thick layers of deposits. Powilleit et al., (2009) studied the response of the polychaete Nephtys hombergii to smothering. This species successfully migrated to the surface of 32-41 cm deposited sediment layer of till or sand/till mixture and restored contact with the overlying water.   While crawling upward to the new sediment surfaces burrowing velocities of up to 20 cm/day were recorded for Nephtys hombergii. Similarly, Bijkerk (1988, results cited from Essink 1999) indicated that the maximal overburden through which species could migrate was 60 cm through mud for Nephtys and 90 cm through sand. No further information was available on the rates of survivorship or the time taken to reach the surface.

Tubificoides spp. and other oligochaetes live relatively deeply buried and can tolerate periods of low oxygen that may occur following the deposition of a fine layer of sediment.  Tubificoides spp. showed some recovery through vertical migration in the same experiment (Bolam, 2011). Whomersley et al., (2010) experimentally buried plots on intertidal mudflats at two sites (Creeksea- Crouch Estuary, England and Blackness- lower Forth Estuary, Scotland), where Tubificoides benedii were dominant species. For each treatment anoxic mud was spread evenly to a depth of 4 cm on top of each treatment plot. The mud was taken from areas adjacent to the plots, and was obtained by scraping off the surface oxic layer and digging up the underlying mud from approximately 20 cm depth. Plots were subject to either low intensity treatments (burial every four weeks) or high (burial every two weeks). The experiment was carried out for 10 months at Creeksea and a year at Blackness. At Creeksea numbers of Tubificoides benedii increased in both burial treatments until the third month (high burial) and sixth month (low burial). At Blackness increased numbers ofTubificoides benedii  were found in both burial treatments after one month (Whomersley et al., 2010).

Laboratory experiments have shown that the snail Hydrobia ulvae can rapidly resurface through 5cm thick fine deposits, although this ability is reduced where deposited sediments contain little water (Chandrasekara & Frid, 1998). Field experiments where 10 cm of sediment were placed on intertidal sediments to investigate the effects of the beneficial use of dredged materials found that the abundance of Hydrobia ulvae had returned to ambient levels within 1 week (Bolam et al., 2004).

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

Pygospio elegans is limited by high sedimentation rates (Nugues et al., 1996) and the species does not appear to be well adapted to oyster culture areas where there are high rates of accumulation of faeces and pseudo faeces (Sornin et al., 1983; Deslous-Paoli et al., 1992; Mitchell, 2006 and Bouchet & Sauriau 2008).  Pygospio elegans is known to decline in areas following re-deposition of very fine particulate matter (Rhoads & Young, 1971; Brenchley, 1981). Experimental relaying of mussels on intertidal fine sands led to the absence of Pygospio elegans compared to adjacent control plots. The increase in fine sediment fraction from increased sediment deposition and biodeposition alongside possible organic enrichment and decline in sediment oxygen levels was thought to account for this (Ragnarsson & Rafaelli, 1999). Bolam (2011) showed that the vertical migration capability of Streblospio shrubsolii was reduced by deposition of just 6 cm of simulated dredged material.

The amphipod Corophium volutator may be sensitive to deposits at the pressure benchmark. Corophium volutator was categorized in AMBI sedimentation Group III – ‘species insensitive to higher amounts of sedimentation, but don’t easily recover from strong fluctuations in sedimentation’ (Gittenberger & Van Loon, 2011). Experimental fences placed on mudflats caused sedimentation rates of 2-2.5 cm/month and reduced Corophium volutator densities from approximately 1700 m² to approximately 400 m². In areas without fences, Corophium volutator numbers increased from approximately 1700 per m² to 3500 per m² (Turk & Risk, 1981 cited in Neal & Avant, 2006). Where a coarse/impermeable layer was added to the seabed the suitability of the habitat for Corophium volutator would be reduced if these could not reach the surface or maintain burrows. Furthermore, a deposition of fine sediment is likely to take several tidal cycles to clear in the low energetic conditions where this biotope occurs.

In intertidal mudflats with similar characterizing species, experiments testing the effects of deposition of sediments typical of beach recharge, have found that recovery of biological assemblages is complete within two years (Bolam & Whomersley, 2003).

Sensitivity assessment. As the exposure to the pressure is for a single discrete event, resistance is assessed as ‘Medium’ as some species associated with the biotope such as Streblospio shrubsolii, Corophium volutator and Pygospio elegans may decline but the biotope is likely to be recognizable within a week due to repositoing and migration of mobile species. Resilience is assessed as ‘High’ and sensitivity is assessed as ‘Low. 

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

Studies have found that beach ‘replenishment’ or ‘nourishment’ that involves the addition of sediments on beaches can have a number of impacts on the infauna (Peterson et al., 2000; Peterson et al., 2006). Impacts are more severe when the sediment added differs significantly in grain size or organic content from the natural habitat (Peterson et al., 2000).

Hediste diversicolor inhabits depositional environments. It is capable of burrowing to depths of up to 0.3 m and reworking sub-surface modifications of its burrow through fine clays and sand. Smith (1955) found no appreciable difference in the population of a Hediste diversicolor colony which had been covered by several inches of sand through which the worms tunnelled. Mobile polychaetes have been demonstrated to burrow through thick layers of deposits. Powilleit et al., (2009) studied the response of the polychaete Nephtys hombergii to smothering. This species successfully migrated to the surface of 32-41 cm deposited sediment layer of till or sand/till mixture and restored contact with the overlying water.   While crawling upward to the new sediment surfaces burrowing velocities of up to 20 cm/day were recorded for Nephtys hombergii. Similarly, Bijkerk (1988, results cited from Essink 1999) indicated that the maximal overburden through which species could migrate was 60 cm through mud for Nephtys and 90 cm through sand. No further information was available on the rates of survivorship or the time taken to reach the surface.

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

The associated species Pygospio elegans is limited by high sedimentation rates (Nugues et al., 1996) and the species does not appear to be well adapted to oyster culture areas where there are high rates of accumulation of faeces and pseudo faeces (Sornin et al., 1983; Deslous-Paoli et al., 1992; Mitchell, 2006 and Bouchet & Sauriau 2008).  Pygospio elegans is known to decline in areas following re-deposition of very fine particulate matter (Rhoads & Young, 1971; Brenchley, 1981). Experimental relaying of mussels on intertidal fine sands led to the absence of Pygospio elegans compared to adjacent control plots. The increase in fine sediment fraction from increased sediment deposition and biodeposition alongside possible organic enrichment and decline in sediment oxygen levels was thought to account for this (Ragnarsson & Rafaelli, 1999). Bolam (2011) showed that Streblospio shrubsolii  vertical migration capability was reduced by deposition of just 6cm simulated dredged material.

The amphipod Corophium volutator may be sensitive to deposits at the pressure benchmark. Experimental fences placed on mudflats that caused sedimentation rates of 2-2.5 cm/month, reduced Corophium volutator densities from approximately 1700 m² to approximately 400 m². In areas without fences,Corophium volutator numbers increased from approximately 1700 per m² to 3500 per m² (Turk & Risk, 1981).

Tubificoides spp. and other oligochaetes live relatively deeply buried and can tolerate periods of low oxygen that may occur following the deposition of a fine layer of sediment.  Tubificoides spp. showed some recovery through vertical migration in the same experiment (Bolam, 2011). Whomersley et al., (2010) experimentally buried plots on intertidal mudflats at two sites (Creeksea- Crouch Estuary, England and Blackness- lower Forth Estuary, Scotland), where Tubificoides benedii were dominant species. For each treatment anoxic mud was spread evenly to a depth of 4 cm on top of each treatment plot. The mud was taken from areas adjacent to the plots, and was obtained by scraping off the surface oxic layer and digging up the underlying mud from approximately 20 cm depth. Plots were subject to either low intensity treatments (burial every four weeks) or high (burial every two weeks). The experiment was carried out for 10 months at Creeksea and a year at Blackness. At Creeksea numbers of Tubificoides benedii increased in both burial treatments until the third month (high burial) and sixth month (low burial). At Blackness increased numbers ofTubificoides benedii  were found in both burial treatments after one month (Whomersley et al., 2010).

In intertidal mudflats with similar characterizing species, experiments testing the effects of deposition of sediments, typical of beach recharge have found that recovery of biological assemblages is complete within two years (Bolam & Whomersley, 2003).

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, although the characterizing species may have some resistance to this to this pressure, populations are likely to be reduced. Resistance to initial smothering is ‘Low’ Resilience is ‘High’ and biotope sensitivity is assessed as ‘Low’.

Litter

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

Evidence

Examples of the impact of specific marine litter, including cigarette butts and micro-plastics are also considered..

Litter, in the form of cigarette butts has been shown to have an impact on ragworms. Hediste diversicolor 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). This UK study suggests health of infauna populations are negatively impacted by this pressure.

Corophium volutator is widely used in ecotoxicological studies and know to uptake nanoplastics, but toxicity at the current environmental relevant concentrations has yet to be confirmed (Booth et al., 2015) However, Corophium volutator forms an important food source for several species of birds and mobile predators such as fish and crabs (Hughes, 1988; Jensen & Kristensen, 1990; Raffaelli et al., 1991; Flach & De Bruin, 1994; Brown et al., 1999), which is likely to result in transition of the particles up the marine food chain. Nevertheless, there was insufficient evidence on which to assess the sensitivity of this biotope to the introduction of litter.

Studies of other characterizing species in relation to micro plastics were not available. However, studies of sediment dwelling, sub surface deposit feeding worms, showed negative impacts from ingestion of micro plastics. For instance, Arenicola marina ingests micro-plastics that are present within the sediment it feeds within. Wright et al. (2013) carried out a lab study that displayed presence of micro-plastics (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 colonisation of sediment by other species, reducing diversity in the biotopes the species occurs within. Wright et al. (2013) also present a case study based on their results, that in the intertidal regions of the Wadden Sea, where Arenicola marina is an important ecosystem engineer, Arenicola marina could ingest 33 m² of micro-plastics a year.

Sensitivity assessment. Marine litter in the form of cigarette butts or micro plastics may impact the health of populations of characterizing species. Significant impacts have been shown in laboratory studies but impacts at biotope scales are still unknown. Evidence and confidence in the assessment is limited 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

There is no evidence on effects of electric and magnetic fields on the characterizing species.

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 levels, confidence in evidence of these effects is very low.

A number of studies have investigated the effects of electromagnetic fields on terrestrial oligochaetes, notable earthworms. Some negative effects have been observed e.g. Tkalec et al., 2013. However no evidence was found to support an assessment at the pressure benchmark for the marine oligochaetes that characterize this biotope.

Field measurements of electric fields at North Hoyle wind farm, North Wales recorded 110µ V/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 potential predators of Hediste diversicolor, thornback ray Raja clavata and attraction to the source in catshark Scyliorhinus canicular (Gill et al. 2009).

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 sensitive to noise and this therefore is ‘Not relevant’.

Introduction of light or shading

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

Evidence

There is little  direct evidence of effects of changes in incident light on the characterizing species of this biotope.  Studentowicz (1936) found that the enchytraeid oligochaete  Enchytraeus albidus, retracted from light, although the worms accumulated at the surface even when illuminated to avoid low oxygen and hydrogen sulpfide.  Giere and Pfannkuche (1982) considered that other enchytraeids and tubificids are likely to react in the same way. As the biological assemblage occurs within the sediment and can be deeply buried (to 10cm or more) this pressure is considered ‘Not relevant’.  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. More general changes to the productivity of the biotope may, however, occur. Beneath shading structures there may be changes in microphytobenthos abundance. Littoral mud and sand support microphytobenthos on the sediment surface and within the sediment. 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

Barriers that reduce the degree of tidal excursion may alter larval supply to suitable habitats from source populations. Conversely, the presence of barriers at 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.Barriers may also act as stepping stones for larval supply over greater distances (Adams et al., 2014).

If a barrier (such as a tidal barrier) incorporated renewable energy  devices such as tidal energy turbines, these devices may affect hydrodynamics and so migration pathways for larvae into and out of the biotope (Adams et al., 2014). Evidence on this pressure is limited.

The trait of Hediste diversicolor to lay and protect eggs within a burrow is likely to limit the impact of barriers to movement on populations. The ability of postlarvae, larger juveniles, and adults of Hediste diversicolor to swim, burrow and be carried by bedload transport can aid the rapid recolonization of disturbed sediments (Shull, 1997).  Davey & George (1986), found evidence that larvae of Hediste diversicolor were tidally dispersed within the Tamar Estuary over a distance of 3 km. A barrier to movement is likely to limit colonization outside the enclosed area, but increase populations within the enclosed area  

Capitella capitata and the associated species Pygospio elegans are capable of both benthic and pelagic dispersal. In the sheltered waters where this biotope occurs, with reduced water exchange, in-situ reproduction may maintain populations rather than long-range pelagic dispersal. As the tubificid oligochaetes that characterize this biotope have benthic dispersal strategies (via egg cocoons laid on the surface (Giere & Pfannkuche, 1982), water transport is not a key method of dispersal over wide distances. 

Sensitivity assessment. Resistance to this pressure is assessed as 'High' and resilience as 'High' by default. This biotope is therefore considered to be 'Not sensitive'.

Death or injury by collision

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

Evidence

‘Not relevant’ to seabed habitats.  NB. Collision by interaction with bottom towed fishing gears and moorings are addressed under

Visual disturbance

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

Evidence

Characterizing species have limited, visual perception, this pressure is therefore considered '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

Important characterizing species within this biotope are not cultivated or translocated. This pressure is therefore 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

Intertidal mixed sediments may be colonized by several invasive non-indigenous species. Invasive species that alter the character of the biotope or that predate on characterizing species are most likely to result in significant impacts. Intertidal flats may be colonized by the invasive non-indigenous species Crepidula fornicata and the pacific oyster Magallana gigas. The two species have not only attained considerable biomasses from Scandinavian to Mediterranean countries but have also generated ecological consequences such as alterations of benthic habitats and communities and food chain changes (OSPAR, 2009b).

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 the decrease in settlement space and an increase in habitat fragmentation because of dense oyster assemblages (Zwerschke et al., 2018).

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

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

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

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

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

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

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

The availability of hard substrata (e.g., gravel) may only restrict initial colonization as higher densities of Crepidula function as substrata for subsequent colonization (Thieltges et al., 2004; Blanchard, 2009). However, Bohn et al. (2015) noted that Crepidula occurred at low density or was absent in areas of homogenous fine sediment and areas dominated by boulders. Bohn et al. (2015) suggested that wave action (exposure) probably prevented the establishment of large numbers of Crepidula in high-energy areas. Blanchard (2009) noted that sandy areas in the Bay of Saint-Mont Michel were not colonized by Crepidula because of surface sand mobility. Thieltges et al. (2003) also noted that storm events removed some clumps of mussels and presumably Crepidula onto tidal flats where they disappeared, which caused their abundance to fluctuate. Similarly, Crepidula was absent from sandy substrata in Swansea Bay but was most abundant in the shelter of the breakwater at the Swansea east site (Powell-Jennings & Calloway, 2018). Powell-Jennings & Calloway (2018) noted that Crepidula is killed by sudden burial and possibly burial due to deposition, which could mitigate Crepidula density. In addition, in the MHW, the highest densities of Crepidula were found in areas of sediment with hard substrata, e.g., mixed fine sediment with shell, 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. Intertidal muddy sands may be exposed to invasive species which can alter the character of the habitat (primarily Crepidula fornicata at the sublittoral fringe and Magallana gigas), leading to re-classification of this biotope. The above evidence suggests that Crepidula fornicata could colonize gravelly sandy mud, typical of this biotope, due to the presence of gravel, pebbles, shells, cobbles, or any other hard substrata that can be used for larvae settlement (Tillin et al., 2020). Therefore, Crepidula has the potential to colonize, and modify the habitat and its associated community due to the introduction of Crepidula shell biomass, silt, pseudofaeces and faeces (Blanchard, 2009; Tillin et al., 2020). Bohn et al. (2015) demonstrated that Crepidula had a preference for gravelly habitats, while De Montaudouin & Sauriau (1999) and Bohn et al. (2015) noted that Crepidula densities were low in intertidal coarse sediments. This habitat is sheltered to extremely sheltered from wave action, which is also suitable for Crepidula colonization. There may be higher densities of Crepidula in the lower shore examples of the biotope, but the densities may be lower in the mid-shore, and it may be absent from the upper shore due to the unsuitable extreme conditions in the intertidal zone preventing Crepidula post-settlement recruitment and mitigating colonization (Bohn et al., 2015). In addition, the reduced salinity levels in this biotope might prevent colonization at high densities, because the majority of evidence records of Crepidula occur in salinities from 30-35 psu (OBIS, 2023). Therefore, resistance to colonization by Crepidula fornicata is assessed as ‘Medium’ and resilience is assessed as ‘Very low’ (because Crepidula would need to be removed), so the biotope sensitivity to Crepidula is assessed as ‘Medium’. Crepidula has not yet been reported to occur in this biotope and there is a lack of direct evidence so the confidence in the assessment is 'Low' and further evidence is required. 

The above evidence suggests that this biotope could be suitable for the colonization of Magallana gigas due to the presence of gravel and other hard substrata required for successful settlement and establishment (Kochmann, 2012; Kochmann et al., 2013; Mckinstry & Jensen, 2013; Herbert et al., 2016; Tillin et al., 2020). The mid-shore to strandline extent or examples of this biotope are 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 high densities due to the abundance of gravel. Therefore, resistance to colonization by Magallana gigas is assessed as 'Low' as a worst case scenario. 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 'High' for gravelly mud biotopes. The confidence in the assessment is 'Low' because the sensitivity of this biotope to Magallana gigas is potentially site-specific.

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 was returned by literature searches on the effect on the key characterizing species, Hediste diversicolor of introduction of relevant microbial pathogens or metazoan disease vectors to an area where they are currently not present.

Corophium volutator is parasitized by several species of trematodes in Europe and North American (McCurdy et al., 2000a; McCurdy et al., 2000b; Mouritsen & Jensen, 1997, cited in Shim et al., 2013). Mass mortalities of Corophium volutator have been associated to infestation by trematodes in the Wadden Sea (Jensen & Mouritsen, 1992). Studies conducted in the Baltic Sea suggested that increased parasitism by trematode species has a detrimental effect on local amphipods (Meissner & Bick, 1999; Mouritsen & Jensen, 1997 cited in Shim et al., 2013).

Sensitivity assessment. Although there are no records of the biotope being affected by the introduction of microbial pathogens in the British Isles, there are reports of mass mortality of characterizing species Corophium volutator (Jensen & Mouritsen, 1992). The sensitivity of the sub-biotope within this group is considered to be higher (see sensitivity assessment for A2.4115, Hediste diversicolor and Corophium volutator in littoral gravelly sandy mud). However, the assessed biotope would not be reclassified, based on a loss of Corophium volutator alone and therefore, resistance is assessed as 'High',  resilience is assessed as 'High' and the biotope is classed as 'Not sensitive' to the introduction of microbial pathogens. Confidence in this assessmentis low as the evidence base is very limited.

Removal of target species

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

Evidence

The sedimentary biotope and characterizing and associated species may be disturbed and damaged by static or mobile gears that are targeting other species. These direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures. The sensitivity assessment for this pressure considers any biological/ecological effects resulting from the removal of target species on this biotope. Ragworms Hediste diversicolor are targeted by recreational and commercial bait diggers. The extent of the impact will depend on the fishing / removal method and spatial extent. 

Populations of Hediste diversicolor are dominated by females; males may constitute up to 40% of the population but several reports suggest that the proportion of males is frequently lower (< 20%) (see Clay, 1967c). The sexes are externally indistinguishable except when approaching maturation and during spawning (see reproduction and adult general biology).

Consequently extraction e.g. by bait digging, of 50% of the specimens from within an area is likely to remove more females than males. A reduction in the female proportion of the population prior to spawning could reduce recruitment to the population. The mechanical action of the digging, even if the worms were not actually taken, may also cause some damage to the bodies. Recovery is dependent on the reproductive success and survival of the remaining population and colonization by adults from unaffected areas.

Sensitivity assessment. The key, characterizing species Hediste diversicolor may be targeted and their removal will alter the character of the biotope. Due to potential impacts on Hediste diversicolor populations, in particular females, biotope resistance is assessed as ‘Low’. Biotope resilience is assessed as ‘High’ and biotope sensitivity is assessed as ‘Low’. 

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, may be damaged or directly removed by static or mobile gears that are targeting other species (see abrasion and penetration pressures). Loss of these species would alter the character of the biotope resulting in re-classification, and would alter the physical structure of the habitat resulting in the loss of the ecosystem functions such as secondary production performed by these species.

Digging for Hediste diversicolor for bait is likely to cause significant mortality of the mud shrimp, Corophium volutator. Bait digging was found to reduce Corophium volutator densities by 39%, juveniles were most affected suffering a 55% reduction in dug areas (Shepherd & Boates, 1999). This would reduce available biomass for higher trophic levels.  Populations of oligochaetes provide food for macroinvertebrates fish and birds. For example up to 67% of flounder and plaice stomachs examined from the Medway estuary (UK) (Van den Broek, 1978) contained the remains of Tubificoides benedii (studied as Peloscolex benedeni) and shrimps which in turn support higher trophic levels (predatory birds and fish). For some migratory birds, the characterizing species Tubificoides benedii can form an important part of the diet during winter (Bagheri & McLusky, 1984). Polychaetes and crustaceans are also predators of oligochaetes and may significantly reduce numbers (Giere & Pfannkuche, 1982 and references therein). The loss of the oligochaete population could, therefore, also impact other trophic levels.

Sensitivity assessment: Loss of the characterizing species of this biotope is likely to occur as by-catch.  Thus, the biotope is considered to have a resistance of 'Low' to this pressure and to have 'High' resilience, resulting in the sensitivity being judged as 'Low'.