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

Lagoon environments are typically shallow (Barnes, 1994) and will, therefore, heat and cool more rapidly than deeper habitats or those that are more connected to the sea and tidally flushed. Species that characterize this habitat are therefore likely to be able to tolerate higher and lower temperatures than open coast species from the shallow subtidal. Populations may be acclimated to the temperatures or able to recover rapidly where populations are impacted.

Arenicola marina is recorded from shores of western Europe, Norway, Spitzbergen, north Siberia, and Iceland. In the western Atlantic, it has been recorded from Greenland, along the northern coast from the Bay of Fundy to Long Island. Its southern limit is about 40°N (see Arenicola marina review), although OBIS (2016) includes a few records from the Atlantic coast of Africa and the Mediterranean. Sommer et al. (1997) examined sub-lethal effects of temperature in Arenicola marina and suggested a critical upper and lower temperature of 20°C and 5°C respectively in North Sea specimens. Above or below these critical temperatures, specimens resort to anaerobic respiration. Sommer et al. (1997) noted that specimens could not acclimate to a 4°C increase above the critical temperature. De Wilde & Berghuis (1979) reported 20% mortality of juveniles reared at 5°C, negligible mortality at 10 and 15°C but 50% mortality at 20°C and 90% at 25°C.

Schroeer et al. (2009) identified a shift in the thermal tolerance of Arenicola marina, with an optimum moving towards higher temperatures with decreasing latitudes, suggesting the species may adapt to long-term shifts such as 2°C but over time. Therefore, Arenicola marina in UK and Irish populations will occupy an optimum temperature range in relation to UK and Irish latitudes. An upper limit above 20°C may occur in more southerly populations. In studies in Whitley Bay, Tyne and Wear, UK, Arenicola marina was most active in spring and summer months, with a mean rate of cast production fastest in spring and particularly slow in autumn and winter, suggesting feeding rate is greatest in higher temperatures (Retraubun et al., 1996). Retraubun et al. (1996) also showed that cast production by specimens in lab experiments increased with temperature, peaking at 20°C before declining. Rates of cast production at 30°C were still higher than at 10°C, suggesting UK populations may have greater tolerance to higher temperatures than populations studied in more northerly latitudes. Temperature changes may affect maturation, spawning time and synchronisation of spawning and reproduction in the long-term (Bentley & Pacey, 1992; Watson et al., 2000). Spawning can be inhibited in gravid adults maintained above 15°C (Watson et al., 2000). However, spawning success would remain dependent upon spring and autumn temperatures remaining below 15°C. Additionally, an impact from temperature change at the substratum surface may be mitigated as Arenicola marina is protected from direct effects by their position in the sediment.

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).

The geographic range of Hediste diversicolor suggests that it is resistant 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 (>20°C) in Black Sea lagoons (Smith, 1977). Hediste diversicolor were not strongly affected by heatwaves in an estuary in north western Portugal, where temperatures may reach 40°C in intertidal pools (higher temperatures than experienced around UK and Irish coasts) (Dolbeth et al. 2011).  Temperature change may adversely affect reproduction. 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 adults die shortly after gamete release.

Deeper burrowing oligochaetes are protected from fluctuations in temperature by the overlaying sediments which dampen changes if poorly drained (Giere & Pfannkuche, 1982).  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. Pygospio elegans were summer visitors to the areas affected by heated effluent. 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 temperature did not influence reproduction strategy (planktotrophy, lecithotrophy or asexual reproduction) but cite Anger (1984) that environmental conditions, including temperature influence timing of reproduction.

Sensitivity assessment. Based on species distributions and evidence for temperature tolerance, the characterizing species are likely to be tolerant of a chronic increase in temperature at the pressure benchmark. Arenicola marina and the associated species are unlikely to be removed entirely but may be impacted by a short-term acute change in temperature of 5°C. Hence, a resistance of Medium is suggested to represent a loss of some of the population. Resilience is probably High and sensitivity is assessed as Low.

Temperature decrease (local)

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

Evidence

Lagoon environments are typically shallow (Barnes, 1994) and will, therefore, heat and cool more rapidly than deepen habitats or those that are more connected to the sea and tidally flushed. Species that characterize this habitat are therefore likely to be able to tolerate higher and lower temperatures than open coast species from the shallow subtidal. Populations may be acclimated to the temperatures or able to recover rapidly where populations are impacted.

Arenicola marina is recorded from shores of western Europe, Norway, Spitzbergen, north Siberia, and Iceland. In the western Atlantic, it has been recorded from Greenland, along the northern coast from the Bay of Fundy to Long Island. Its southern limit is about 40°N (see Arenicola marina review), although OBIS (2016) includes a few records from the Atlantic coast of Africa and the Mediterranean.

Arenicola marina displays a greater tolerance to decreases in temperature than to increases, although optimum temperatures are reported to be between 5°C and 20°C. Reise et al. (2001) stated that Arenicola marina was known to be a winter hardy species and that its abundance and biomass were stable even after severe winters.  Sommer et al. (1997) report populations in the White Sea (sub-polar) acclimatised to -2°C in winter. Populations in the North Sea (boreal) were less tolerant of temperatures below 5°C, although in laboratory experiments on individual lugworms from North Sea populations worms survived a temperature drop from 6 or 12°C to -1.7°C for more than a week (Sommer & Portner, 1999).

Temperature change may affect maturation, spawning time and synchronisation of spawning and reproduction in the long-term (Bentley & Pacey, 1992; Watson et al., 2000). Spawning success is dependent upon spring and autumn temperatures, the seasons when spawning occurs in relation to spring and neap tides, remaining below 13-15°C. De Wilde & Berghuis (1979) reported 20% mortality of juveniles reared at 5 °C, negligible mortality at 10 °C and 15 °C but 50% at 20°C and 90% mortality at 25°C.

Evidence from the Sylt in the North Sea suggests that the effects of severe winters on Arenicola marina populations are small and brief (Reise, et al., 2001) The severe winter of 1995/1996 disrupted the usual juvenile settlement cycle in the sand flats of the Sylt, North Sea (Reise et al., 2001).  In the severe winter, the adult population of Arenicola marina migrated down the shore, to deeper, waters to avoid low temperatures and 66 days of ice on the intertidal sand flats.  Although, the adult population was halved, and no dead lugworms were observed on the surface or in the sediment. The post-larvae hibernate in the deep water channels (subtidal) in shell gravel and mussel beds. In summer the juveniles were not restricted to the upper shore but settled over a wider area of the flats, in the space left by the adult population. Reise et al. (2001) concluded that the enhanced recruitment demonstrated that the post-larvae did not suffer increased mortality during the winter, probably as their subtidal hibernation sites did not experience ice cover.  Similarly, Arenicola marina was listed as ‘apparently unaffected’ by the severe 1962/63 winter in the UK (Crisp, 1964).

The geographic range of Hediste diversicolor suggests that it is resistant 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 (>20°C) in Black Sea lagoons (Smith, 1977).

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).

Crisp (1964) reported that species of amphipod and isopods seemed to be unharmed by the severe winter of 1962-1963. This may be due to burial in sediments buffering temperature or seasonal migration to deeper waters to avoid freezing. 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).

Sensitivity assessment. Arenicola marina and the populations of other species present in the biotope are distributed to the north of the British Isles, exhibit regional acclimation to temperature, are known to be winter hardy, and can migrate to deeper waters or within sediments to avoid change in temperature and even ice.  Therefore, the biotope is probably resistant of a short to long-term decrease in temperature at the benchmark level and a resistance of High is suggested. Hence, resilience is High and the biotope is assessed as Not sensitive at the benchmark level.

Salinity increase (local)

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

Evidence

This biotope occurs in reduced (18-35 pp) and low (<18 ppt) salinity (JNCC, 2015). Biotopes that occur in low salinity are considered tolerant of an increase to reduced salinity as this falls within the habitat range. A change at the pressure benchmark is assessed as a change to full salinity. Species in lagoons may be able to tolerate some fluctuations in salinity as evaporation on hot days may increase salinity and tidal flushing may lead to some changes.

Arenicola marina loses weight when exposed to hyperosmotic shock (47 psu for 24 hrs) but are able to regulate and gain weight within 7-10 days (Zebe & Schiedek, 1996).

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. Hylleberg (1975) also found that under controlled conditions of salinity ranging from 10 to 30ᵒ⁄ₒₒand temperatures ranging from 5 to 35° C, shows that Hydrobia ulvae has maximal egestion at the combination of high salinity (30ᵒ⁄ₒₒ) 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.

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.  The characterizing species are able to survive in both fully marine and brackish water and may be unaffected by an increase in salinity (although some acclimation may be required). As salinity is a key structuring factor it is likely that a long-term change in salinity would alter the biological assemblage allowing species that are intolerant of low and reduced salinity to colonize. Biotope resistance is therefore assessed as Low and resilience as Medium, so that sensitivity to this pressure is assessed as Medium.

Salinity decrease (local)

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

Evidence

This biotope occurs in reduced (18-35 pp) and low (<18 ppt) salinity (JNCC, 2015). Biotopes that occur in reduced salinity are considered tolerant of a change to low as this fall within the habitat range. A change at the pressure benchmark is assessed as a change to freshwater. Few of the characterizing species are likey to tolerate a long-term salinity reduction at the pressure benchmark. Biotope resistance is therefore assessed as None and resilience as Medium (following habitat recovery). Biotope sensitivity is therefore assessed as Medium.

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

This biotope is found in very weak tidal conditions where water flow is weak (<0.5 m/s) negligible (JNCC, 2015).  An increase in water flow at the benchmark is unlikely to have a significant negative effect on the biological composition of the biotope as many of the characterizing species are found in biotopes that are exposed to stronger tidal streams.  However, it must be assumed that if there is an increase in the water flow within the biotope there will also be an increase in the water flow around the lagoon.  An increase or decrease in the water flow at the pressure benchmark may result in increased erosion of sands or deposition of fine silts resulting in changes in sediment composition.  An increase in water flow above the level of the benchmark this could consequently lead to the loss/collapse of a lagoon wall and completely change the physical environment of the biotope, and lead to the loss of the lagoon biotope altogether. Decreased water flow may also have implications for oxygenation and larval transport as water exchange and flushing are reduced. General predictions are limited as the change will depend on site-specific factors such as the structure of the lagoon, the degree of water exchange and sediment supply.

Sensitivity assessment.  The biotope occurs in weak to very weak flow so that any further reduction is not relevant. An increase in water flow could modify the sediment. A significant increase may result in a change in the sediment from fine muds to sand muds and the fine particulates are removed.  The experimental evidence suggests that a change in the flow of 0.11 m/s to 0.25 m/s was enough to alter the sediment and the appearance of the biotope within 65 days. Therefore, a reduction in flow of 0.1-0.2 m/s may alter the sediment and the appearance of the biotope resulting in a change to the mud lagoon SS.SMu.SMuLS. Therefore, a resistance of None is suggested. Resilience is probably High as, once the low energy conditions return, it may only take a couple of years for the mud to deposit in these otherwise sheltered and isolated habitats. Hence, sensitivity is assessed as Medium.

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

Changes in emergence is only relevant to intertidal and sublittoral fringe biotopes.

Wave exposure changes (local)

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

Evidence

This biotope is found in extremely sheltered conditions.  An increase or decrease in wave exposure at the benchmark is unlikely to have a significant negative effect on the biological composition of the biotope.  However, it might be assumed that if there is an increase in the wave height within the biotope there will also be an increase in the water flow around the lagoon.  This increase could have a detrimental effect on the structure of the lagoon through erosion.  This could consequently lead to the loss collapse of a lagoon wall and completely change the physical environment of the biotope, and lead to the loss of the lagoon biotope altogether.

Sensitivity assessment.  Wave exposure can have a significant structuring effect on biotopes through direct effects on species and indirectly through changes in sediment composition and transport and physical disturbance. As lagoons are sheltered from waves a change at the pressure benchmark is very small. Resistance and resilience are assessed as ‘High’ and the biotope is assessed as ‘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.

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.

Corophium volutator is highly intolerant of metal pollution at levels often found in estuaries from industrial outfalls and contaminated sewage. A concentration 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., 1985b). 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).

Sediment may act as a sink for heavy metals contamination so that deposit feeding species may be particularly vulnerable to heavy metal contamination through ingestion of particulates. At high concentrations of Cu, Cd or Zn the blow lug left the sediment (Bat & Raffaelli, 1998). The following toxicities have been reported in Arenicola marina:

• no mortality after 10 days at 7 µg Cu/g sediment, 23 µg Zn/g and 9 µg Cd/g;
• median lethal concentrations (LC₅₀) of 20 µg Cu/g, 50 µg Zn/g, and 25 µg Cd/g (Bat & Raffaelli, 1998).

Bryan (1984) suggested that polychaetes are fairly resistant to heavy metals, based on the species studied. Short-term toxicity in polychaetes was highest to Hg, Cu and Ag, declined with Al, Cr, Zn and Pb whereas Cd, Ni, Co and Se the least toxic.

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.

Sheltered embayments and lagoons, where this biotope is found, are particularly vulnerable to oil pollution, which may settle onto the sediment and persist for years (Cole et al., 1999). Subsequent digestion or degradation of the oil by microbes may result in nutrient enrichment and eutrophication (see nutrients below). Although protected from direct smothering by oil by its depth, the biotope is relatively shallow and would be exposed to the water soluble fraction of oil, water soluble PAHs, and oil adsorbed onto particulates.

Suchanek (1993) reviewed the effects of oil spills on marine invertebrates and concluded that, in general, on soft sediment habitats, infaunal polychaetes, bivalves and amphipods were particularly affected. Crude oil and oil: dispersant mixtures were shown to cause mortalities in Arenicola marina (see review). Prouse & Gordon (1976) found that blow lug was driven out of the sediment by waterborne fuel oil concentrations of >1 mg/l or sediment concentration of >100 µg/g. Crude oil and refined oils were shown to have little effect on fertilization in sea urchin eggs but in the presence of dispersants, fertilization was poor and embryonic development was impaired (Johnston, 1984). Sea urchin eggs showed developmental abnormalities when exposed to 10-30mg/l of hydrocarbons and crude oil : Corexit dispersant mixtures have been shown to cause functional loss of tube feet and spines in sea urchins (Suchanek, 1993). Although no direct information on synaptid holothurians was found, it seems likely that adults and especially larvae are intolerant of hydrocarbon contamination.

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.

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 xenobiotic ivermectin was used to control parasitic infestations in livestock including sea lice in fish farms, degrades slowly in marine sediments (half-life >100 days). Ivermectin was found to produce a 10 day LC50 of 18µg ivermectin /kg of wet sediment in Arenicola marina. Sub-lethal effects were apparent between 5 - 105 µg/kg. Cole et al. (1999) suggested that this indicated a high intolerance. Arenicola marina has shown negative responses to chemical contaminants, including damaged gills following exposure to detergents (Conti, 1987), and inhibited the action of esterases following suspected exposure to point source pesticide pollution in sediments from the Ribble estuary, UK (Hannam et al., 2008).

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 affectCorophium 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 rephasing 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

Reports on littoral sediment benthic communities at Sandside Bay, adjacent to Dounray nuclear facility, Scotland, (where radioactive particles have been detected and removed) reported Arenicola marina were abundant (Dounray Particle Advisory Group, 2008). Kennedy et al. (1988) reported levels of ¹³⁷Cs in Arenicola spp. of 220-440 Bq/kg from the Solway Firth.  However, no information on the effects of radionuclide contamination was found.

Introduction of other substances

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

Evidence

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

Species that are likely to be sensitive to de-oxygenation at the pressure benchmark are Pygospio elegans and Corophium volutator. 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.  In a series of experiments Gamenick et al., (1996)  suggested that 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 results are largely in concordance with other work by Gamble (1970) who found that survival rates were temperature dependent with individuals surviving longer at lower temperatures.  The level of oxygen was not assessed by Gamenick et al., 1996) and the description of the experimental set-up suggests that anoxic test conditions were used rather than hypoxic. Gamble (1970)  found that at 5^oC most individuals were inactive after 30 minutes exposure to anaerobic seawater and that mortality occurred later, the inactivity may have allowed the species to survive longer (Gamble, 1970).

Other species within the biotope are more tolerant of hypoxia. 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).

Arenicola marina is subject to reduced oxygen concentrations regularly at low tide and is capable of anaerobic respiration. The transition from aerobic to anaerobic metabolism takes several hours and is complete within 6-8 hrs, although this is likely to be the longest period of exposure at low tide. Fully aerobic metabolism is restored within 60 min once oxygen returns (Zeber & Schiedek, 1996). This species was able to survive anoxia for 90 hrs in the presence of 10 mmol/l sulphide in laboratory tests (Zeber & Schiedek, 1996). Hydrogen sulphide (H₂S) produced by chemoautotrophs within the surrounding anoxic sediment and may, therefore, be present in Arenicola marina burrows. Although the population density of Arenicola marina decreases with increasing H₂S, Arenicola marina is able to detoxify H₂S in the presence of oxygen and maintain a low internal concentration of H₂S. At high concentrations of H₂S in the lab (0.5, 0.76 and 1.26 mmol/l) the lugworm resorts to anaerobic metabolism (Zeber & Schiedek, 1996). At 16°C Arenicola marina survived 72 hrs of anoxia but only 36 hrs at 20°C. Tolerance of anoxia was also seasonal, and in winter anoxia tolerance was reduced at temperatures above 7°C. Juveniles have a lower tolerance of anoxia but are capable of anaerobic metabolism (Zebe & Schiedek, 1996). However, Arenicola marina has been found to be unaffected by short periods of anoxia and to survive for 9 days without oxygen (Borden, 1931 and Hecht, 1932 cited in Dales, 1958; Hayward, 1994). Diaz & Rosenberg (1995) listed Arenicola marina as a species resistant of severe hypoxia.

Sensitivity assessment.  Burrowing species such as Arenicola marina, Hediste diversicolor and the oligochaetes burrow into the anoxic sediments found in this biotope (JNCC, 2015) and may be tolerant of hypoxia.  Species that occur at the surface and that are frequently found in well-oxygenated sandy sediments such as Pygospio elegans and Corohpium volutator are likely to be more sensitive. At the pressure benchmark biotope resistance is assessed as Low based on the loss of some characterizing species, biotope resilience is assessed as High and sensitivity is Low.

Nutrient enrichment

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

Evidence

The abundance and biomass of Arenicola marina increase with increased organic content in their favoured sediment (Longbottom, 1970; Hayward, 1994). Therefore, moderate nutrient enrichment may be beneficial.

Indirect effects may include algal blooms and the growth of algal mats (e.g. of Ulva sp.) on the surface of the intertidal flats. Algal mats smother the sediment, and create anoxic conditions in the sediment underneath, changes in the microphytobenthos, and with increasing enrichment, a reduction in species richness, the sediment becoming dominated by pollution tolerant polychaetes, e.g. Manayunkia aestuarina. In extreme cases, the sediment may become anoxic and defaunated (Elliot et al., 1998). Algal blooms have been implicated in mass mortalities of lugworms, e.g. in South Wales where up to 99% mortality was reported (Boalch, 1979; Olive & Cadman, 1990; Holt et al. 1995). Feeding lugworms were present and exploitable by bait diggers within 1 month, suggesting rapid recovery, probably by migration from surrounding areas or juvenile nurseries.

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

Organic enrichment

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

Evidence

This biotope is characterized by species that are exclusively deposit feeders or that can switch to deposit feeding, including Arenicola marina, Hediste diversicolor, Pygospio elegans, oligochaetes and Corophium volutator. An input of organic matter may provide a food subsidy for these species.

The abundance and biomass of Arenicola marina increase with increased organic content in their favoured sediment (Longbottom, 1970; Hayward, 1994). Moderate enrichment increases food supplies, enhancing productivity and abundance. Gray et al. (2002) concluded that organic deposits between 50 to 300 gC m^–2 yr^–1, are efficiently processed by benthic species. Substantial increases > 500 g C m^-2 yr^-1 would likely to have negative effects, limiting the distribution of organisms and degrade the habitat, leading to eutrophication, algal blooms, and changes in community structure to a community dominated by opportunist species (e.g. capitellids) with increased abundance but reduced species richness, and eventually to abiotic anoxic sediments (Pearson & Rosenberg, 1978; Gray, 1981; Snelgrove et al.,1995; Cromey et al., 1998).

Borja et al. (2000) and Gittenberger & Van Loon (2011) placed Arenicola marina into the AMBI pollution group III, defined as ‘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)’.

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.  The biotope is probably rich in organic matter as it occurs in sheltered, isolated areas.  An input of organic matter at the pressure benchmark is likely to provide food for deposit feeders within the biotope. Therefore, a resistance of High is suggested at the benchmark level. Hence, resilience is High and the biotope is assessed as Not sensitive at the benchmark level.

Physical loss (to land or freshwater habitat)

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

Evidence

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

Physical change (to another seabed type)

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

Evidence

The biotope is characterized by the sedimentary lagoon habitat (JNCC, 2015), so a change to an artificial or rock substratum would alter the character of the biotope leading to reclassification and the loss of the sedimentary community including the characterizing oligochaetes and polychaetes that live buried within the sediment.

Sensitivity assessment. Based on the loss of the biotope, resistance is assessed as ‘None’, recovery is assessed as ‘Very low’ (as the change at the pressure benchmark is permanent), and sensitivity is assessed as ‘High’.

Physical change (to another sediment type)

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

Evidence

 A change in sediment type by one Folk class (using the Long 2006 simplification) would change the sediment to sand or mixed sediments. Although many of the characterizing species are likely to persist, the biotope would probably be re-classified to the sublittoral sand lagoon type SS.SSa.SSaLS or the mixed sediment SS.SMx.SMxLS.  A change to coarse sediments would significantly alter species composition through loss of Arenicola marina and amphipods and oligochaetes and other associated species. Therefore, a resistance of None is recorded, resilience is Very low (the pressure is a permanent change) and sensitivity is assessed as High.

Habitat structure changes - removal of substratum (extraction)

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

Evidence

Sedimentary communities are likely to be highly intolerant of substratum removal, which will lead to partial or complete defaunation, exposing underlying sediment which may be anoxic and/or of a different character or bedrock and lead to changes in the topography of the area (Dernie et al., 2003). Any remaining species, given their new position at the sediment/water interface, may be exposed to conditions to which they are not suited. Removal of 30 cm of surface sediment will remove the polychaete and oligochaete community and other species present in the biotope. Recovery of the biological assemblage may take place before the original topography is restored, if the exposed, underlying sediments are similar to those that were removed.

Sensitivity assessment. Extraction of 30 cm of sediment will remove the characterizing biological component of the biotope. Resistance is assessed as ‘None’ and biotope resilience is assessed as ’Medium’. Biotope sensitivity is therefore ‘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

Abrasion and compaction of the surficial layer may damage individuals, species that live close to the surface or move on the surface such as Pygospio elegans and Corophium volutator are likely to be more sensitive than species that burrow deeply into sediments such as Hediste diversicolor, oligochaetes and Arenicola marina.

Arenicola marina lives in sediment to a depth of 20-40 cm and is, therefore, protected from most sources of abrasion and physical disturbance caused by surface action. However, it is likely to be damaged by any activity (e.g. anchors, dredging) that penetrates the sediment (see below). 

There are few studies on the effects of trampling on sedimentary habitats. Most studies suggest that the effects of trampling across sedimentary habitats depend on the relative proportion of mud to sand (sediment porosity), the dominant infauna (nematodes and polychaetes vs. bivalves) and the presence of burrows (Tyler-Walters & Arnold, 2008). Recovery from impact is relatively fast as shown by Chandrasekara & Frid (1996), where no difference was reported between samples in winter following summer trampling. Wynberg & Branch (1997) suggest that trampling effects are most severe in sediments dominated by animals with stable burrows, as these collapse and the sediment becomes compacted. Rossi et al. (2007) examined trampling across intertidal mudflats but were not able to show a significant difference in Arenicola abundance between trampled and control sites due to the natural variation in abundance between study sites. 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.

Sensitivity assessment. Abrasion may damage or kill a proportion of the population of the characterizing  and associated species. Arenicola marina and Tubificoides spp. that are generally buried more deeply within sediments are likely to be more resistant than species such as Pygospio elegans that inhabit fragile tubes that extend above the sediment surface. Biotope resistance is assessed as Medium and resilience as High, so 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

Disturbance of the sediment below the surface may affect all the characterizing infauna and a number of studies demonstrate effects on the characterizing species.

Mendonça et al. (2008) studied populations of the polychaete Arenicola marina at Culbin Sands lagoon, Moray Firth, in NE Scotland. An unprecedented and unexpected cockle harvesting event took place,1.5 years after the start of the sampling programme, which dramatically disturbed the sediment as it was conducted using tractors with mechanical rakes in some areas, and by boats using a suction dredge in other areas. Therefore, there was an opportunity to compare annual biomass fluctuations “before” and “after” the disturbance. Arenicola marina was observed to return to normal activities just a few hours after the disturbance of the sediment during the harvesting event.

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).

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 m⁻²) 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 (surpassing the study monitoring timeline).

Kaiser et al. (2001) carried out experimental hand raking, similar to that used in inter tidal cockle fisheries. Both small and large raked plots showed changed communities in comparison to control plots, smaller plots recovered in 56 days, whilst larger plots remained in an altered state. A three-fold damage rate for undersized cockles was recorded in hand-raked plots compared to control plots.

The extraction of cockles by sediment raking and mechanical disturbance and digging for lugworms causes significant mortality of 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).

Sensitivity assessment.  Penetrative gear would probably damage or remove a proportion of the population of Arenicola marina and the characterizing oligochaetes but given potential density, the effects may be minor.  Other characterizing species including Pygospio elegans and Corophium volutator may be damaged and suffer high levels of mortality. Hence, a resistance of Low is suggested. Resilience is probably Medium, due to the isolated nature of the sea lochs and lagoons in which this biotope if found, and sensitivity is assessed as Medium.

Changes in suspended solids (water clarity)

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

Evidence

This biotope occurs in low energy environments (wave sheltered and weak flow) in shallow isolated water bodies.  Deposit feeders are unlikely to be perturbed by increased concentrations of suspended sediment since they live in sediment and are probably adapted to re-suspension of sediment by wave action, during storms or runoff.

In 36-65 day mesocosm studies of the effects of Arenicola marina bioturbation, Wendelboe et al. (2013) found that the surface of the sediment was dominated by faecal mounds and feeding pits at a flow rate of 0.11 m/s, but was more eroded and the surface was more even at 0.25 m/s. At the low flow (0.11 m/s) there was no change in the sediment. However, at 0.25 m/s, there was a substantial reduction in the silt and clay fractions of the sediment (a 36% reduction) and in the organic content of the sediment (a 42% reduction). At 0.25 m/s the material ejected into faecal casts was eroded (once the mucilaginous coating had eroded) and the water surface became turbid, resulting in loss of both silt/clay fractions and organic matter.  

Sensitivity assessment.  The evidence from Wendelboe et al. (2013) suggests that an increase in water movement due to storms, or runoff is likely to disturb the sediment surface regularly, especially in winter months, so that the biotope is probably not affected by changes in suspended sediment.  In addition, Arenicola marina occurs at high abundances in mudflats and sandflats in estuaries where suspended sediment levels may reach grammes per litre. Therefore, a resistance of High is suggested so that resilience is High (by default) and the biotope is assessed as Not sensitive at the benchmark level.

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

Arenicola marina is a sub-surface deposit feeder that derives the sediment it ingests from the surface. It rapidly reworks and mixes sediment. It grows to 12-20 cm in length and lives in burrows to a depth of 20-40 cm. It is unlikely to be perturbed by smothering by 5 cm of sediment. Juveniles may be more susceptible but both adults and juveniles are capable of leaving the sediment and swimming (on the tide) up or down the shore (see Reise et al., 2001). In addition, Gittenberger & Van Loon (2011) placed Arenicola marina into their AMBI Sedimentation Group III, defined as ‘species insensitive to higher amounts of sedimentation, but don’t easily recover from strong fluctuations in sedimentation’.

Sensitivity assessment. This biotope occurs in a depositional environment, where sedimentation is likely, to be high due to the low energy of the habitat. Therefore, resistance to a deposit of 5 cm of fine sediment is assessed as High. Hence, resilience is High (by default) and the biotope is probably Not sensitive at the benchmark level.

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

Arenicola marina is a sub-surface deposit feeder that derives the sediment it ingests from the surface. It rapidly reworks and mixes sediment. It grows to 12-20 cm in length and lives in burrows to a depth of 20-40 cm. Adults may be able to resist smothering by 30 cm of sediment but juveniles may be more susceptible.  Both adults and juveniles are capable of leaving the sediment and swimming (on the tide) up or down the shore (see Reise et al., 2001). In addition, Gittenberger & Van Loon (2011) placed Arenicola marina into their AMBI sedimentation Group III, defined as ‘species insensitive to higher amounts of sedimentation, but don’t easily recover from strong fluctuations in sedimentation’.

Sensitivity assessment. This biotope occurs in a depositional environment, where sedimentation is likely, to be high due to the low energy of the habitat. However, the deposit of 30 cm in a single event is probably greater than the normal range of sedimentation and, in theses sheltered habitats, likely to remain.  Therefore, a proportion of the adults and a greater proportion of the juveniles may not be able to realign themselves with the surface of the sediment and resistance is assessed as Medium but at ‘Low’ confidence due to the lack of direct evidence. Hence, resilience is probably High and sensitivity is assessed as Low at the benchmark level.

Litter

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

Evidence

DNA damage when exposed to water with toxicants (present in cigarette butts) in quantities 60 fold lower than reported from urban run-off (Wright et al., 2015). Studies are limited on impacts of litter on infauna and this UK study suggests health of infauna populations are negatively impacted by this pressure.

Studies of sediment dwelling, sub surface deposit feeding worms, a trait shared by species abundant in this biotope, 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 decreased bioturbation levels. These effects 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 33mᵌ; of micro plastics a year.

In a similar experiment, Browne et al. (2013) exposed Arenicola marina to sediments with 5% PVC particles or sand presorbed with pollutants nonylophenol and phenanthrene for 10 days. PVC is dense and sinks to the sediment. The experiment used Both microplastics and sand transferred the pollutants into the tissues of the lugworm by absorption through the gut. The worms accumulated over 250% more of these pollutants from sand than from the PVC particulates. The lugworms were also exposed to PVC particulates presorbed with plastic additive, the flame retardant PBDE-47 and antimicrobial Triclosan. The worms accumulated up to 3,500% of the concentration of theses contaminants when compared when to the experimental sediment. Clean sand and PVC with contaminants reduced feeding but PVC with Triclosan reduced feeding by over 65%. In the PVC with Triclosan treatments 55% of the lugworms died.  Browne et al., 2013 concluded that the contaminants tested reduced feeding, immunity, response to oxidative stress, and survival (in the case of Triclosan).

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

Electromagnetic changes

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

Evidence

No evidence was found

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 into the sediment for protection. However, at the benchmark level, the community is unlikely to be respond to noise and therefore is Not sensitive.

Introduction of light or shading

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

Evidence

All characterizing species live in the sediment and do not rely on light levels directly to feed or so limited direct impact is expected. As this biotope is not characterized by the presence of primary producers it is not considered that shading would alter the character of the habitat directly.

Beneath shading structures, there may be changes in microphytobenthos abundance. This biotope may 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 deposit feeders like Arenicola and synaptid holothurians, although they fed on a range of organic matter within the sediment.

Sensitivity assessment. Therefore, biotope resistance is assessed as ‘High’ and resilience is assessed as ‘High’ (by default) and the biotope is considered to be ‘Not sensitive’.

Barrier to species movement

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

Evidence

Not relevant - this pressure is considered applicable to mobile species, e.g. fish and marine mammals rather than seabed habitats. 

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. 

Visual disturbance

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

Evidence

Not relevant.

Genetic modification & translocation of indigenous species

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

Evidence

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

Introduction or spread of invasive non-indigenous species

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

Evidence

The 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). 

Sensitivity assessment. The sediments characterizing this biotope are likely to be too mobile and unsuitable for most of the invasive non-indigenous species currently recorded in the UK. The above evidence suggests that this biotope is unsuitable for the colonization of Crepidula fornicata due to a lack of gravel, shells, or any other hard substrata used for larvae settlement (Tillin et al., 2020). This habitat occurs in extremely sheltered lagoons which could be suitable for Crepidula, but the reduced and low salinity levels in the biotope might mitigate or prevent colonization at high densities. The majority of evidence records Crepidula in salinities from 25-35 psu (OBIS, 2023). Hence, resistance is assessed as 'High' and resilience as 'High' so that the biotope is assessed as 'Not sensitive'.

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

Ashworth (1904) recorded the presence of distomid cercariae and Coccidia in Arenicola marina from the Lancashire coast. However, no information concerning infestation or disease related mortalities was found.

In the Danish Wadden Sea, a dense field of Corophium volutator disappeared completely, and the density of the mud snail Hydrobia ulvae declined by 40 % during spring 1990 as a result of an epizootic by trematodes. High spring temperature accelerated both the development rate and the release of infective larval stages of an infectious trematode from the snail. This event coincided with a high positive NAO index, high temperatures, strong winds, and increased precipitation in northern Europe (Mouritsen & Poulin, 2002a, and references therein). The transmission rates of larval parasites from snail to amphipods and the rate of parasite‐induced amphipod mortality are both strong positive functions of temperature (Jensen & Mouritsen, 1992; Mouritsen, 2002). Using a simulation model, Mouritsen et al. (2005) demonstrated that a 3.8 °C increase in ambient temperature would probably result in a parasite induced collapse of the amphipod population in the Wadden Sea.

Marine oligochaetes host numerous protozoan parasites without apparent pathogenic effects even at high infestation levels  (Giere & Pfannkuche, 1982 and references therein)

Sensitivity assessment.  Outbreaks of pathogens and parasites may occur in this biotope and lead to changes in species abundance and composition. Biotope resistance is assessed as ‘Medium’ as the evidence suggests that infections are species-specific and changes in abundance are unlikely to result in biotope classification. Resilience is assessed as ‘High’ and biotope sensitivity is assessed as ‘Low’.

Removal of target species

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

Evidence

Within this biotope the polychaetes Arenicola marina and Hediste diversicolor may be targeted recreationally or commercially. McLusky et al. (1983) examined the effects of bait digging on blow lug populations in the Forth estuary. Dug and infilled areas and unfilled basins left after digging re-populated within 1 month, whereas mounds of dug sediment took showed a reduced population. The basins accumulated fine sediment and organic matter and showed increased population levels for about 2-3 months after digging.

Fowler (1999) reviewed the effects of bait digging on intertidal fauna, including Arenicola marina. Diggers were reported to remove 50 or 70% of the blow lug population. Heavy commercial exploitation in Budle Bay in winter 1984 removed 4 million worms in 6 weeks, reducing the population from 40 to <1 per m². Recovery occurred within a few months by recolonization from surrounding sediment (Fowler, 1999). However, Cryer et al. (1987) reported no recovery for 6 months over summer after mortalities due to bait digging. Mechanical lugworm dredgers were used in the Dutch Wadden Sea where they removed 17-20 million lugworms/year. However, when combined with hand digging the harvest represented only 0.75% of the estimated population in the area. A near doubling of the lugworm mortality in dredged areas was reported, resulting in a gradual substantial decline in the local population over a 4 year period. The effects of mechanical lugworm dredging are more severe and can result in the complete removal of Arenicola marina (Beukema, 1995; Fowler, 1999). Beukema (1995) noted that the lugworm stock recovered slowly reached its original level in at least three years.

Smaller scale extraction of patches of substratum through activities such as bait digging for Hediste diversicolor may have impacts over finer spatial scales within the biotope. If the impact is not spread over a larger area the effects are likely to occur within the dug area.

Corophium species are affected by sediment disturbance from deposit feeders (Flach, 1992) and removal of Arenicola marina may be beneficial for these species. The activities of Arenicola marina also reduce the abundance of Pygospio elegans (Wilson, 1981).

Sensitivity assessment.  Recreational bait digging may remove a proportion of the population of Hediste diversicolor and Arenicola. The physical effects of removal are addressed under penetration above. Arenicola marina is a bioturbator and ecosystem engineer and its removal would probably have a significant effect on the nature of the sediment and the other species that could inhabit the sediment. As both species are relatively sedentary and targeted removal is likely to remove large proportions of the population, a resistance of Low is suggested. Resilience is probably Medium, due to the isolated nature of the sea lochs and lagoons in which this biotope if found, and sensitivity is assessed as Medium. This biotope occurs in the sublittoral fringe and this may limit targeted removal where the biotope is never exposed during the tidal cycle.

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

Incidental removal of the characterizing species would alter the character of the biotope and the delivery of ecosystem services such as secondary production and bioturbation. Arenicola marina is a bioturbator and ecosystem engineer and its incidental removal would probably have a significant effect on the nature of the sediment and the other species that could inhabit the sediment. 

Many lagoons are important feeding areas for birds (Barnes, 1994) and removal of species such as Hydrobia ulvae and Corophium spp. will alter food supply. Fish may also feed on bivalve siphons and tails of Arenicola marina (Barnes, 1994). The removal of Ruppia and other vegetation will remove refugia enhancing predation on species (Barnes, 1994). 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). 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, impact other trophic levels.

Sensitivity assessment. Removal of the characterizing species would alter the character of the biotope. Resistance is therefore assessed as ‘Low’ and resilience as ‘Medium’ so that sensitivity is categorised as ‘Low’.