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

In shallow sea lochs, sedimentary biotopes typically experience seasonal changes in temperature between 5°C and 15°C (Hughes, 1998a). Although unusually warm summers or cold winters may change the temperatures outside this range, benthic burrowing species will be buffered from extremes by their presence in the sediment.

Callianassa subterranea is recorded from the Norwegian coasts of North Sea, south through the Bay of Biscay to the Mediterranean (OBIS, 2016). In the North Sea, Callianassa subterranea lives in water temperatures that vary between 6 and 15°C (Rowden et al., 1998). Calocaris macandreae is abundant in muddy sediments around the British east and west coasts, extending from Scandinavia to West Africa and the Mediterranean (Ingle & Christiansen 2004; cited in Pinn & Atkinson, 2010). Nephrops norvegicus is distributed from Iceland to the eastern Mediterranean at temperatures between 6 and 17°C (Eriksson et al., 2013; Johnson et al., 2013).   Hernroth et al. (2012) exposed individuals from a population found in the Skagerrak to temperature elevations 4°C above normal for the area for four months.  No signs of oxidative stress were observed and mortality rates were not affected.  Maxmuelleria lankesteri is recorded from the Irish Sea, Clyde Sea, Scottish sea lochs, the Kattegat and Skagerrak and north-west Spain (Hughes, 1998a).

Sensitivity assessment.  Short-term acute changes in temperature and long-term chronic changes in temperature at the pressure benchmark are considered unlikely to adversely this biotope as global distribution suggest Nephrops norvegicus, Calocaris macandreae and Callianassa subterranea can potentially adapt to a wide range of temperatures experienced in both northern and southern waters.  While Maxmuelleria lankesteri has a more limited distribution it would probably be able to avoid locally acute changes in temperature as they burrow deeply into the sediment.  Therefore, resistance and resilience are assessed as  High. This biotope is, therefore, considered to be Not sensitive. 

Temperature decrease (local)

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

Evidence

In shallow sea lochs, sedimentary biotopes typically experience seasonal changes in temperature between 5°C and 15°C (Hughes, 1998a). Although, unusually warm summers or cold winters may change the temperatures outside this range, benthic burrowing species will be buffered from extremes by their presence in the sediment.

Callianassa subterranea is recorded from the Norwegian coasts of North Sea, south through the Bay of Biscay to the Mediterranean (OBIS, 2016). In the North Sea, Callianassa subterranea lives in water temperatures that vary between 6 and 15°C (Rowden et al., 1998). Calocaris macandreae is abundant in muddy sediments around the British east and west coasts, extending from Scandinavia to West Africa and the Mediterranean (Ingle & Christiansen 2004; cited in Pinn & Atkinson 2010). Nephrops norvegicus is distributed from Iceland to the eastern Mediterranean at temperatures between 6 and 17°C (Eriksson et al., 2013; Johnson et al., 2013).   Hernroth et al. (2012) exposed individuals from a population found in the Skagerrak to temperature elevations 4°C above normal for the area for four months.  No signs of oxidative stress were observed and mortality rates were not affected.  Maxmuelleria lankesteri is recorded from the Irish Sea, Clyde Sea, Scottish sea lochs, the Kattegat and Skagerrak and north-west Spain (Hughes, 1998a).

Sensitivity assessment.  Short-term acute changes in temperature and long-term chronic changes in temperature at the pressure benchmark are considered unlikely to adversely this biotope as global distribution suggest Nephrops norvegicus, Calocaris macandreae and Callianassa subterranea can potentially adapt to a wide range of temperatures experienced in both northern and southern waters.  While Maxmuelleria lankesteri has a more limited distribution it would probably be able to avoid locally acute changes in temperature as they burrow deeply into the sediment.  Resistance is, therefore, assessed as High and resilience as High.  This group is therefore considered to be Not sensitive. 

Salinity increase (local)

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

Evidence

No evidence was found to assess salinity tolerance of Calocaris macandreae.  It is found in fully marine conditions.  No habitat records from estuaries or brackish water were found.  Similarly, Callianassa subterranea and Maxmuelleria lankesteri are only recorded from full (30-35) saline conditions.

Thompson & Ayers (1989) noted that Nephrops larvae were found at salinities of 34-35 ppt in the wild. Johnson et al. (2013) noted that Nephrops was generally restricted to full salinity waters, considered stenohaline, and was recorded by OBIS from 31.8 to 38.8 psu.  Farmer (1975) reported that Nephrops occurred at salinities of 29-30 ppt in the Kattegat and 35.8-38.7 ppt in the Adriatic. However, Höglund (1942; cited in Farmer, 1975) suggested that the absence of Nephrops norvegicus in the Baltic Sea was due to its intolerance to very low salinities.

The effects of low salinity exposure and emersion were tested to simulate the conditions experienced by discarded Nephrops in the Kattegat area as these are transported through the halocline (Harris & Ulmestrand, 2004).  Nephrops exposed to 15 psu (for <2 hr) suffered mortalities of 25-42% overall.  Exposed animals gained mass rapidly as water was absorbed and showed delayed or absent responses to stimulation following return to waters of 33 psu.(Harris & Ulmestrand, 2004; Johnson et al., 2013).  In addition, Nephrops was reported to survive at 28 psu but experience 50% mortality 25 psu and 100% mortality at 21 psu (Harris & Ulmestrand, 2004).

An increase in salinity at the benchmark level, would result in a salinity of >40 psu, and as hypersaline water is likely to sink to the seabed, the biotope may be affected by hypersaline effluents. Ruso et al. (2007) reported that changes in the community structure of soft sediment communities due to desalinisation plant effluent in Alicante, Spain. In particular, in close vicinity to the effluent, where the salinity reached 39 psu, the community of polychaetes, crustaceans and molluscs was lost and replaced by one dominated by nematodes. Roberts et al. (2010b) suggested that hypersaline effluent dispersed quickly but was more of a concern at the seabed and in areas of low energy where widespread alternations in the community of soft sediments were observed. In several studies, echinoderms and ascidians were amongst the most sensitive groups examined (Roberts et al., 2010b).

Sensitivity assessment.  An increase in salinity from full to >40 psu is probably detrimental to the important characteristic species of the biotope. Hypersaline water would probably sink to the seabed and potentially into the sediment via burrows. Although, there is no direct evidence of the effects of hypersaline water, the stenohaline nature of the community suggests that hypersaline conditions may cause mortality. Therefore, a resistance of Low is recorded but at Low confidence.  Resilience would probably be Low, so that sensitivity may be High.

Salinity decrease (local)

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

Evidence

No evidence was found to assess salinity tolerance of Calocaris macandreae.  It is found in fully marine conditions. No habitat records from estuaries or brackish water were found.  Similarly, Callianassa subterranea and Maxmuelleria lankesteri are only recorded from full (30-35) saline conditions.

Thompson & Ayers (1989) noted that Nephrops larvae were found at salinities of 34-35 ppt in the wild. Johnson et al. (2013) noted that Nephrops was generally restricted to full salinity waters, considered stenohaline, and was recorded by OBIS from 31.8 to 38.8 psu.  Farmer (1975) reported that Nephrops occurred at salinities of 29-30 ppt in the Kattegat and 35.8-38.7 ppt in the Adriatic. However, Höglund (1942; cited in Farmer, 1975) suggested that the absence of Nephrops norvegicus in the Baltic Sea was due to its intolerance to very low salinities.

The effects of low salinity exposure and emersion were tested to simulate the conditions experienced by discarded Nephrops in the Kattegat area as these are transported through the halocline (Harris & Ulmestrand, 2004).  Nephrops exposed to 15 psu (for <2 hr) suffered mortalities of 25-42% overall.  Exposed animals gained mass rapidly as water was absorbed and showed delayed or absent responses to stimulation following return to waters of 33 psu.(Harris & Ulmestrand, 2004; Johnson et al., 2013).  In addition, Nephrops was reported to survive at 28 psu but experience 50% mortality 25 psu and 100% mortality at 21 psu (Harris & Ulmestrand, 2004).

Sensitivity assessment.  A decrease in salinity from full to reduced (18-30 psu) is likely to be detrimental to most of the important characteristic species in the biotope. Callianassa subterranea, Calocaris macandreae and Maxmuelleria lankesteri are only recorded from full (30-35) saline conditions. The above evidence shows that short, acute reductions in salinity result in mortality in Nephrops, but also that reduced salinity results in mortality. Therefore, a reduction is salinity for a year is likely to either cause the mobile species to move out of the affected area or cause significant mortality. Therefore, a resilience of Low is recorded. Resilience would probably be Low, so that sensitivity may be High. It is noted that many Scottish sea lochs in which this biotope is recorded may experience variable salinity conditions but the hyposaline conditions probably do not occur at the depths this community occurs.

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 occurs in weak to very weak (negligible) flow, in deep low energy environments. A further decrease in water flow is unlikely.  Nephrops has been shown to walk in line with water flow between 0.07 and 0.2 m/s in flume experiments (Newell et al., 1988) but no other direct evidence of the effects of changes in water flow was found.  Increased flow has the potential to modify the sediment, especially at the surface. A significant increase in water flow may winnow away mud surface or even remove the mud habitat and hence the biotope if prolonged. An increase of 0.2 m/s may begin to erode the mud surface where the site is already subject to flow (e.g. weak flow at the seabed), based on sediment erosion deposition curves (Wright et al., 2001).  However, given the depth of mud that characterizes the biotope only the surface of the mud may be removed within a year. Hence, the deep burrowing community may remain intact but the surface infauna and erect epifauna may reduce in abundance. Therefore, a resistance of Medium is recorded but with Low confidence.  Resilience is probably Medium and sensitivity of the biotope is assessed 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 are Not relevant to the biotope, which is restricted to circalittoral below 10 metres. The pressure benchmark is relevant only to littoral and shallow 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

SS.SMu.CFiMu.MegMax occurs in low-energy environments, extremely sheltered to sheltered from wave exposure (Connor et al., 2004), a prerequisite for the fine mud sediments in which the community is found (Hughes, 1998). In addition, the biotope is found to considerable depths, at which, wave action is unlikely to be significant. Therefore, a decrease in wave exposure is 'Not relevant'. Any activity or climatic effect that increased wave action or storminess could have a significant effect on the shallower examples of the biotope, due to removal or modification of the sediment. However, a change of 3-5% in significant wave height (the benchmark) is unlikely to be significant. Therefore, the biotope is probably 'Not sensitive' (resistance and resilience are High) at the benchmark level.

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.

In Norwegian fjords, Rygg (1985) found a relationship between species diversity in benthic fauna communities and sediment concentrations of the heavy metals Cu, Pb, and Zn. Cu, in particular, showed a strong negative correlation and the author suggested a cause-effect relationship. Those species not present at sites where Cu concentrations were greater than ten times higher than the background level, such as Calocaris macandreae, Amphiura filiformis and several bivalves including Nucula sulcata and Thyasira equalis, were assessed as non-tolerant species. The tolerant species were all polychaete worms. Therefore, increased heavy metal contamination in sediments may change the faunal composition of the community and decrease overall species diversity. Some burrowing crustaceans, brittlestars, and bivalves may disappear from the biotope and lead to an increasing dominance of polychaetes.

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 biotope is recorded as This pressure is Not assessed but evidence is presented where available.

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.

In the fish farming industry, a range of synthetic compounds has been used treat parasitic infestations in the past. Ivermectin, an anti-louse treatment, was shown to be highly toxic to sediment-dwelling polychaetes (Black et al., 1997; Thain et al., 1997), epibenthic shrimps (Burridge & Haya, 1993) and also thought to be toxic to burrowing megafauna (Hughes, 1998a). The pesticide carbamyl (1-naphthol n-methyl carbamate; trade name Sevin®) has been used to control populations of thalassinidean mud-shrimps in areas important for oyster cultivation (Feldman et al., 2000).

Radionuclide contamination

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

Evidence

Burrowing fauna probably have a major influence on the distribution of radionuclides within the sediments (Kershaw et al., 1983). Maxmuelleria lankesteri burrows may act as sinks for surface-derived radionuclides and there is probably little return of deeply-buried material to the sediment surface (Hughes et al., 1996). Plutonium is reported to accumulate in the linings of Maxmuelleria lankesteri burrows, this emphasises the role of bioturbation in the incorporation of radionuclides in deeper sediments (Kershaw et al., 1984). Communities similar to this biotope containing abundant burrowing megafauna and sea pens were found to exist in areas heavily contaminated by radionuclides, in particular near Sellafield, Cumbria, due to the activities of the British Nuclear Fuels Plc reprocessing plant (Hughes & Atkinson, 1997) but no information on the level of radiation was provided.  No reports on the effects on the fauna themselves were found. Therefore, the biotope is may be resistant of such effluent but there is insufficient evidence to assess this pressure against the benchmark.

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

Crustaceans are thought to be amongst the most susceptible group to the effects of hypoxia (Diaz & Rosenberg, 1995; Vaquer-Sunyer & Duarte, 2008; Eriksson et al., 2103). Large, active animals with high respiratory demands are likely to be most affected by oxygenation changes, whereas burrow-dwelling fauna may be less susceptible to hypoxic conditions. The oxygen concentrations in Nephrops grounds was reported to be between 6 and 9.4 mgO₂/l and in Scottish sea lochs has been reported to range from 1 -9.2 mgO₂/l (Gilibrand et al., 2006; Eriksson et al., 2013). Oxygen depletion can occur naturally (warm temperatures combined with prolonged stratification of the water column), however, it can also be caused by human activities such as sewage disposal, cage aquaculture or eutrophication.

Diaz & Rosenberg (1995) suggested that Nephrops norvegicus was sensitive to hypoxia. Nephrops norvegicus is sensitive to extreme hypoxia (0.6 mg O₂/l), but in moderately hypoxic conditions (1 mg O₂/l) can compensate by increasing haemocyanin levels (Baden et al., 1990).

In the laboratory, juvenile Nephrops behaviour and mortality changed with lowered oxygen concentrations; energetically costly activities were reduced, and activity in general declined. In normoxia, juveniles initially walked and then burrowed but when exposed to hypoxia they were mainly inactive with occasional outbursts of escape swimming. To increase oxygen availability the juveniles were observed to raise their bodies on stilted legs (similar to adults in hypoxic conditions) but an oxygen saturation of 25% (<2.5 mg O₂/l) were lethal within 24 h (Eriksson & Baden, 1997). Burrowing behaviour was tested in post-larvae at an oxygen saturation of >80% (<8 mg O₂/l) for 1 wk. The difference in time taken to complete a V-shaped depression or a U-shaped burrow was measured and showed a strong negative relationship between post larval age and burrowing time but all individuals made a burrow. Eriksson & Baden (1997) suggested that juveniles were, therefore, more sensitive to hypoxia than adults.

In moderately hypoxic conditions 38-43% saturation (3.8-4.3 mg O₂/l) adult Nephrops norvegicus compensates by increasing production of haemocyanin (Baden et al., 1990). In the laboratory, this compensation lasted one week so at the level of the benchmark, the species would not be killed. However in severe hypoxia, <20% saturation (<2 mg/l) Nephrops became less active and raised their bodies on their legs (Baden et al., 1990). During laboratory studies at <15% O₂ (1.5mg O₂/l) specimens of Nephrops norvegicus stopped feeding even though there was available food suggesting that hypoxia induces starvation (Baden et al., 1990).  At 12% (<1.2 mg O₂/l) oxygen saturation some specimens of Nephrops norvegicus began to 'tip toe'. They supported themselves by elevating the body from the substratum with their claws and telson. The lobsters remained elevated until they became tired, sluggish, and barely moved when touched for 2-3 days after which they died (Baden et al., 1990). At <10% (<1 mg O₂/l) adult Nephrops died within a few days (Baden et al., 1990; Eriksson et al., 2013).

Nephrops leave their burrows at <50% O₂ (at 1 m above the substratum) or <15% O₂ (at 0.5 m above the substratum) (Eriksson et al., 2013). Catches of Nephrops norvegicus were found to be high in hypoxic conditions, probably because the animals are forced out of their burrows (Eriksson & Baden, 1997). Baden et al. (1990) reported that the Nephrops biomass declined from 10.8 kg/hr to zero from October 1984 to September 1989 in the SE Kattegat, an area affected by 1-3 month periods of low oxygen concentrations (< 2ml/l = 2.8 mg/l) during the 1980s. Eriksson et al. (2013) suggested that increased temperatures due to climate change may increase hypoxic stress on benthos as median lethal oxygen concentration increases with temperature.

The bioturbative activity of burrowing megafauna improves ventilation and oxygenation of burrows. Thalassinidean mud-shrimps are very resistant to oxygen depletion and many species can survive extended periods of anoxia of 50-60 hr at 10°C (Anderson et al., 1994).  Callianassa subterranea burrows are often hypoxic or even anoxic (Hughes, 1998a). In laboratory experiments, the species survived for up to five days under anoxic conditions at 6°C (Powilleit & Graf, 1996). The species has several adaptations that allow it to survive in low oxygen environments: a low rate of oxygen consumption, large gill areas and a respiratory pigment with a high oxygen affinity (Astall et al., 1997; Taylor et al., 2000). However, anoxic, sulphide-rich waters upwelling in a Norwegian fjord (Christiansen & Stene, 1998; cited in Hughes, 1998a) killed Callianassa subterranea.

Calocaris macandreae also in habitats burrows subject to severe hypoxia. In the laboratory, Calocaris macandreae was highly tolerant of anoxia, with a LT₅₀ of 43 hr (although some specimens survived for 49.5 hrs), as it exhibited anaerobic metabolism at severe hypoxia (PO₂ <7 Torr, or ca 0.4 mg O₂/l) (Anderson et al., 1994).

Mud shrimps are among the few species to survive the low oxygen partial pressures and high sulphide levels in the vicinity of fish cages in sea lochs (Atkinson, 1989). In Caol Scotnish, Loch Sween, bacterial mats of Beggiatoa were reported in the immediate vicinity of salmon cages in 1987. The burrowing megafauna (Maxmuelleria lankesteri, Callianassa subterranea and Jaxea nocturna) were abundant in unimpacted areas. However, by 1988, the bacterial mats covered most of the seabed in the basin, the sediment was close to anoxic, and the burrows of megafauna were restricted to small areas free of Beggiatoa. After the removal of salmon cages in 1989, some recovery was apparent by 1990 with more burrows apparent, although the size of the individuals of Maxmuelleria lankesteri, Callianassa subterranean suggested that they had survived the loch basin during the peak of enrichment (Atkinson, 1989; Hughes, 1998a). Little other evidence on the tolerance of Maxmuelleria lankesteri to deoxygenation was found. However, it is thought to be tolerant of hypoxic conditions, as burrow conditions often become hypoxic (Hughes, 1998a).

In experiments exposing benthic invertebrates to decreasing oxygen levels, Amphiura chiajei only left its protected position in the sediment when oxygen levels fell below 0.54 mg O₂L^-1 (Rosenberg et al., 1991). This escape response increases its risk to predators. Mass mortality in a superficially similar species of ophiuroid, Amphiura filiformis from the south-east Kattegat has been observed during severe hypoxic events (< 0.7 mg/l), while the abundance of Amphiura chiajei remained unchanged at the same site and time (Rosenberg & Loo, 1988).

Sensitivity assessment. Therefore, a decrease in oxygenation to 2 mg/l or below for a week (the benchmark), is likely result in mortality of Nephrops due to an increase in predation or fishing mortality, or direct mortality due to severe hypoxia. The mud shrimp fauna and Maxmuelleria lankesteri may survive severe hypoxia or even anoxia in a short period or one week (the benchmark). Amphiura chiajei abundance in the biotope may also not be affected adversely until exposed to severe hypoxic conditions. However, a reduction in the abundance of Nephrops is unlikely to change to the character of the biotope as the other important characteristic species are likely to remain. Therefore, a resistance of Medium is suggested. As the Nephrops population would probably recover within 2-10 year, resilience is likely to be Medium, and, hence, sensitivity is assessed as Medium.

Nutrient enrichment

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

Evidence

Burrowing megafauna flourish is areas where the sediments are naturally high in organic matter and, hence nutrients, such as sheltered sea lochs (Hughes, 1998a). For example, Nephrops norvegicus was present in high densities in Loch Sween, Scotland where the organic content was about 5% and as high as 9% in some patches (Atkinson, 1989). Callianassa subterranea is found in sediments with a range of organic content. In the soft, organically enriched sediments (typical organic carbon values of 3.6 - 7.8%) of Loch Sween, a sea loch in Scotland, Callianassa subterranea was present as a significant megafaunal burrower (Atkinson, 1989). The maximum depth of the species burrows has been recorded as 86 cm, which Nickell & Atkinson (1995) suggest is an underestimate, indicates a nutritional requirement for sub-surface organic matter. In the North Sea, where sediments have a low organic content Rowden & Jones (1997) found Callianassa subterranea had to construct much more complex burrows to support their energetic costs.

An increasing gradient of organic enrichment (e.g. in the vicinity of point sources of organic-rich effluent or sewage sludge dump sites) results in a decline in the suspension feeding fauna and an increase in the number of deposit feeders, in particular, polychaete worms (Pearson & Rosenberg, 1978). The effects of organic enrichment on burrowing megafauna and other infauna depended on the degree of enrichment and any resultant hypoxia, which depend on the sediment type and local hydrology.  For example, is a survey of Garoch Head sludge dumping grounds, Firth of Clyde, the burrowing megafauna (Nephrops norvegicus, Callianassa subterranean, Calocaris macandreae, Lumpenus lampraetiformis and Cepola rubsecens) were abundant where organic content was <4% but absent where the organic content exceeded 6% (Smith, 1988, cited in Hughes, 1998a). Calocaris macandreae did not extend as far into the gradient as Nephrops norvegicus or Lumpenus lampraetiformis (Smith, 1988, cited in Hughes, 1998a). In Caol Scotnish, Loch Sween, bacterial mats of Beggiatoa were reported in the immediate vicinity of salmon cages in 1987. The burrowing megafauna (Maxmuelleria lankesteri, Callianassa subterranea and Jaxea nocturna) were abundant in unimpacted areas. But by 1988, the bacterial mats covered most of the seabed in the basin, the sediment was close to anoxic, and the burrows of megafauna were restricted to small areas free of Beggiatoa. After the removal of salmon cages in 1989, some recovery was apparent by 1990 with more burrows apparent, although the size of the individuals of Maxmuelleria lankesteri, Callianassa subterranean suggested that they had survived the loch basin during the peak of enrichment (Hughes, 1998a).

Hoare & Wilson (1977) noted that Virgularia mirabilis was absent from part of the Holyhead Harbour heavily affected by sewage pollution.  However, the species was abundant near the head of Loch Harport, Skye, close to a distillery outfall discharging water enriched in malt and yeast residues and other soluble organic compounds (Nickell & Anderson, 1977; cited in Hughes, 1998a), where the organic content of the sediment was up to 5%.  Virgularia mirabilis was also present in Loch Sween in Scotland in sites where organic content was as high as 4.5% (Atkinson, 1989).

Nevertheless, this biotope is recorded as 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

Burrowing megafauna flourish in areas where the sediments are naturally high in organic matter, such as sheltered sea lochs (Hughes, 1998a). For example, Nephrops norvegicus was present in high densities in Loch Sween, Scotland where the organic content was about 5% and as high as 9% in some patches (Atkinson, 1989). Callianassa subterranea is found in sediments with a range of organic content. In the soft, organically enriched sediments (typical organic carbon values of 3.6 - 7.8%) of Loch Sween, a sea loch in Scotland, Callianassa subterranea was present as a significant megafaunal burrower (Atkinson, 1989). The maximum depth of the species burrows has been recorded as 86 cm, which Nickell & Atkinson (1995) suggest is an underestimate, indicating a nutritional requirement for sub-surface organic matter. In the North Sea, where sediments have a low organic content Rowden & Jones (1997) found Callianassa subterranea had to construct much more complex burrows to support their energetic costs.

An increasing gradient of organic enrichment (e.g. in the vicinity of point sources of organic-rich effluent or sewage sludge dump sites) results in a decline in the suspension-feeding fauna and an increase in the number of deposit feeders, in particular, polychaete worms (Pearson & Rosenberg, 1978). The effects of organic enrichment on burrowing megafauna and other infauna depended on the degree of enrichment and any resultant hypoxia, which depend on the sediment type and local hydrology.  For example, is a survey of Garoch Head sludge dumping grounds, Firth of Clyde, the burrowing megafauna (Nephrops norvegicus, Callianassa subterranean, Calocaris macandreae, Lumpenus lampraetiformis and Cepola rubsecens) were abundant where organic content was <4% but absent where the organic content exceeded 6% (Smith, 1988, cited in Hughes, 1998a). Calocaris macandreae did not extend as far into the gradient as Nephrops norvegicus or Lumpenus lampraetiformis (Smith, 1988, cited in Hughes, 1998a). In Caol Scotnish, Loch Sween, bacterial mats of Beggiatoa were reported in the immediate vicinity of salmon cages in 1987. The burrowing megafauna (Maxmuelleria lankesteri, Callianassa subterranea and Jaxea nocturna) were abundant in unimpacted areas. But by 1988, the bacterial mats covered most of the seabed in the basin, the sediment was close to anoxic, and the burrows of megafauna were restricted to small areas free of Beggiatoa. After the removal of salmon cages in 1989, some recovery was apparent by 1990 with more burrows apparent, although the size of the individuals of Maxmuelleria lankesteri, Callianassa subterranean suggested that they had survived the loch basin during the peak of enrichment (Hughes, 1998a).

Hoare & Wilson (1977) noted that Virgularia mirabilis was absent from part of the Holyhead Harbour heavily affected by sewage pollution.  However, the species was abundant near the head of Loch Harport, Skye, close to a distillery outfall discharging water enriched in malt and yeast residues and other soluble organic compounds (Nickell & Anderson, 1977; cited in Hughes, 1998a), where the organic content of the sediment was up to 5%.  Virgularia mirabilis was also present in Loch Sween in Scotland in sites where organic content was as high as 4.5% (Atkinson, 1989).

Sensitivity assessment. Sublittoral muds may be expected to be high in organic nutrients.  The characteristic burrowing megafauna are probably resistant to all but gross enrichment.  Therefore, a precautionary resistance of Medium is suggested, and as resilience is probably Medium, a sensitivity of Medium is recorded.

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

If sedimentary substrata were replaced with rock substrata the biotope would be lost, as it would no longer be a sedimentary habitat and would no longer support sea pens and burrowing megafauna.

Sensitivity assessment. Resistance to the pressure is considered ’None‘, and resilience ’Very low‘ or ‘None’ (as the pressure represents a permanent change) and the sensitivity of this biotope 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

Species creating permanent burrows typically have specific sediment requirements, relating to the maintenance of burrow structures. Callianassa subterranea creates a complex lattice of galleries at 30-40 cm below the surface in the fine muds but burrows less deeply (9-23 cm) in coarse sediments (Rowden & Jones, 1995; Hughes, 1998a).  Calocaris macandreae creates burrows with a total depth of 21 cm in muddy sediments with a high silt content but is not found in sandy sediments (Buchanan, 1963; Hughes, 1998a). The large echiuran Maxmuelleria lankesteri burrows up to 80 cm into the sediment and is found in fine muds and muddy sands in deep water (10-80 m) (Nickell et al., 1995; Hughes, 1998a).

Nephrops norvegicus burrows to 20-30 cm and is found in soft mud sediments (Hughes, 1998a). Nephrops has been shown to be more frequent in sandy muds than muds off the southwest and southeastern grounds off Portugal (Leotte et al., 2005; abstract only). In coarse, sandy sediments, population density is low because of the instability of the sediment and the tendency of burrows to collapse.   In medium-grained mud sediments, Nephrops are able to construct stable burrows, and population density peaks. In very fine-grained, soft muds, Nephrops excavate extensive burrow complexes, and competition for space is a limiting factor on population density (Afonso-Dias, 1998).

The important characterizing burrowing megafauna occur in a relatively restricted range of sediment types, related to the burrowing life habit (and feeding for Calocaris macandreae). The species are, therefore considered, to have ‘Low’ resistance to a change in sediment type of one Folk class for a year. However, resilience is Very low or ‘None’ (as the pressure represents a permanent change). Sensitivity is, therefore, assessed as High.

Habitat structure changes - removal of substratum (extraction)

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

Evidence

No direct evidence was found to assess the impacts of this pressure. Callianassa subterranea creates a complex lattice of galleries at 30-40 cm below the surface in the fine muds but burrows less deeply (9-23 cm) in coarse sediments (Rowden & Jones, 1995; Hughes, 1998a).  Calocaris macandreae creates burrows with a total depth of 21 cm in muddy sediments with as high silt content (Buchanan, 1963; Hughes, 1998a); Maxmuelleria lankesteri burrows up to 80 cm into the sediment (Nickell et al., 1995; Hughes, 1998a); and Nephrops norvegicus burrows to 20-30 cm and is found in soft mud sediments (Hughes, 1998a). Based on burrow depths (maximum depth 21 cm for Calocaris macandreae and 30 cm for Nephrops norvegicus) extraction (of 30 cm of sediment) is likely to disturb and remove the majority of the population of Calocaris macandreae and Nephrops norvegicus, together with a proportion of the Callianassa subterranea population within the affected area. A proportion of the Maxmuelleria lankesteri population may remain, depending on their depth within the sediment.  Resistance is assessed as None (removal of >75% of individuals) and recovery is assessed as Low. Sensitivity is, therefore, assessed as High. Confidence in the quality of evidence for this assessment is Low as it is based on expert judgement, informed by life habit of the species assessed.

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

Species living in deep subtidal mud habitats are considered to be more vulnerable to physical disturbance as they are adapted to stable conditions (Pommer et al., 2016).  In general, species with large body size, low dispersal, late maturation and long lifespan are considered sensitive to physical disturbance (Bolam et al., 2014; Pommer et al., 2016). Similarly, sessile epifauna and species that live at or near the sediment surface are likely to be more vulnerable to physical disturbance than deep-burrowing or mobile species (Pommer et al., 2016). Large bioturbating or bio-irrigating species may be especially sensitive and their loss may affect the community (Widdicombe et al., 2004; Pommer et al., 2016).

Hinz et al. (2009) noted that different studies on the effects of otter trawl disturbance in muddy sediments gave mixed results and that the effect on abundance, biomass and diversity at a community level were largely inconsistent between studies. For example, experimental studies on short-term effects showed modest changes in the benthic communities (e.g. Tuck et al., 1998) and meta-analysis suggested that otter trawling on muddy sediments had one of the least negative impacts on the benthos (Kaiser et al., 2006). However, other studies showed that areas of seabed protected by wrecks from Nephrops trawls had higher abundance and biomass of benthos (Ball et al., 2000), while Smith et al. (2000) showed significantly lower abundance, biomass and species richness of benthos in high-intensity trawling lanes. Hinz et al. (2009)  suggested that the differences in results were the result of differences in statistical analysis, prior fishing intensity and duration of the studies. Hinz et al. (2009) reported that chronic otter trawling from a Nephrops fishery had significant negative effects on the benthic macrofauna. Hinz et al. (2009) concluded that while the initial impact of otter trawl on muddy sediments was modest, the long-term disturbance could lead to profound changes in the benthic communities, especially epifauna and shallow burrowing infauna.

Nephrops norvegicus fisheries could, therefore, affect burrowing megafauna and sea pen biotopes. Nephrops is a commercially targeted species that is harvested by static and mobile gears. Information on the European fisheries for this species is summarised by Ungfors et al. (2013). It is difficult to conduct stock assessments on Nephrops, which can only be harvested selectively by trawls and static gears. Nephrops cannot be aged directly. European Nephrops fisheries are managed as Functional Units (FUs), which are smaller than the usual ICES sub-regions due to the limited dispersal abilities of Nephrops. The estimates of abundance, and hence the recommended maximum sustainable yield (MSY), the related Biomass trigger points and fishing mortality (F_MSY), estimated harvest rates and ICES recommended limits on landings and by-catch vary between FUs, (Ungfors et al., 2013; Marine Scotland, 2016).  For example, harvest rates (ratio of total catch to absolute abundance) vary from ca 5-25% between 2007 and 2015 in the Farn Deeps, to ca 5-30% between 2005 and 2015 in South Minch (Marine Scotland, 2016). Marine Scotland (2016) suggested that the abundance of most stocks in the North Sea has declined to the MSY Biomass trigger point but remained above the F_MSY trigger point. However, in West Scotland, most stocks are above the Biomass trigger point but fluctuate around the F_MSY (Marine Scotland, 2016). Nevertheless, landings of Nephrops in 2014 were 13,700 tonnes in the North Sea and 12,800 in West Scotland (Marine Scotland, 2016).

Nephrops trawls catch specimens that are foraging at the surface. Trawl-caught Nephrops females were reported to have fewer eggs on average than creel-caught females from the same area, during an experimental study, and that it was likely that the eggs may be lost due to physical abrasion (Chapman & Ballantyne, 1980). The proportion of eggs lost to abrasion ranged from 11-22% in samples taken from the Clyde and West of Kintyre (Chapman & Ballantyne, 1980).  The entrances to Nephrops burrows are likely to be damaged by abrasion. However, Marrs et al. (1998) reported that burrows were re-established within 2 days providing that the occupant had remained unharmed (Marrs et al., 1998). Nevertheless, burrow density was lower in frequently trawled areas of Loch Fyne except in areas protected from trawling by submarine obstructions (Howson & Davies, 1991; Hughes, 1998a). Video studies have found that only a low proportion (circa 5%) of Nephrops that approached creels to enter them (Bjordal, 1986; Adey, 2007, cited in Ungfors et al., 2013).  Factors that govern emergence will influence catch rates as only individuals that have emerged from burrows will be caught by trawl hauls.  The degree of emergence from burrows for feeding or mating appears to be mainly governed by light intensities and therefore depends on factors such as time of day and season and varies between populations at different depths (Katoh et al., 2013).  Experimental trawling (Bell et al., 2008) to evaluate catch rates showed that catchability varied between vessels in the same area and that catch rates were strongly linked to tidal cycles with increased catch rates at spring rather than neap tides. Catch rates differ between genders (Ungfors et al., 2013); berried females tend to stay within burrows and are rarely caught in trawls (Aguzzi and Sarda 2008, cited in Katoh et al., 2013). The population of Nephrops in the Irish Sea, in muds between the Isle of Man and the Irish coast, may be an exception.  The area is subject to a near-surface gyre that retains larvae in the vicinity of the adults, so that while the population is self-sustaining, it may be vulnerable to over-exploitation as it is unlikely to receive recruitment from the surrounding area (Hill et al., 1996b, 1997b; Hughes, 1998a).  Hughes (1998a) noted that areas that were unsuitable for trawling due to rocky outcrops or other obstacles were often exploited by creeling. Hughes (1998a) suggested that trawling could reduce the density of Nephrops in confined sea lochs but cited Atkinson’s observation that the resilience of Nephrops populations to trawling is enhanced by the fact that juveniles and egg-bearing females remain in their burrows and are not caught by trawls.

Calocaris macandreae is suggested to rarely venture onto the surface (Nash et al. 1984).  Bergmann et al. (2002) noted that small numbers of Calocaris macandreae were by-catch in Nephrops trawls in the Clyde Sea. Comparisons between grab samples collected at trawled and untrawled sites in the Oslofjord, a northern branch of the Skagerrak in the North Sea, showed that Calocaris macandreae were depleted at trawled sites. The mean abundance of Calocaris macandreae was 41.5 individuals per m² (ca ±9.91) in non-trawled areas and 14.5 individuals per m² (ci.±4.99) in trawled areas (Olsgard et al., 2008). Trawled areas were visited by otter trawlers targeting Pandalus montagui between 50 and 100 times per year, and based on the size of the trawls and the boat speed, each part of these areas are trawled on average 2–3 times per year (Olsgard et al., 2008).  It is not clear whether the impact is cumulative with decreases in the population occurring incrementally or if the first pass removes the most vulnerable individuals, and those that remain are either new recruits or individuals that are more resistant due to factors such as burrow depth. However, Pommer et al. (2016) did not find a significant difference in the abundance of Calocaris macandreae with trawling intensity in the Kattegat. Duineveld et al. (2007) reported a higher species diversity and abundance of mud shrimps (Callianassa subterranea and Upogebia deltura) with a fisheries exclusion zone in the North Sea than in the surrounding area.

Bolam et al. (2014) suggested that spoon worms (Echiura) of the family Bonellidae (the family to which Maxmuelleria lankesteri belongs) had a high sensitivity to trawling based on their average sensitivity score from eight traits (mainly body size, morphology, lack of mobility, longevity and low recruitment) in their biological traits analysis. However, the depth of the burrows constructed by characterizing megafauna (mud-shrimps and Maxmuelleria lankesteri) probably protects the species from surface abrasion and fishing activities. For example, Maxmuelleria lankesteri burrows up to 80 cm into the sediment (Nickell et al., 1995; Hughes, 1998a); Callianassa subterranea creates a complex lattice of galleries at 30-40 cm below the surface in the fine muds but burrows less deeply (9-23 cm) in coarse sediments (Rowden & Jones, 1995; Hughes, 1998a); Calocaris macandreae creates burrows with a total depth of 21 cm in muddy sediments with a high silt content (Buchanan, 1963; Hughes, 1998a); and Nephrops norvegicus burrows to 20-30 cm and is found in soft mud sediments (Rice and Chapman 1971; Nash et al. 1984; Hughes, 1998a). Based on burrow depths surface abrasion is unlikely to likely to disturb or remove the majority of the population of Maxmuelleria lankesteri, Calocaris macandreae, Callianassa subterranea, or Nephrops norvegicus within the affected area, although the proboscis of Maxmuelleria lankesteri could be damaged by passing gear at night.

The burrow opening may be damaged (as above) but observations from Loch Sween suggest that they are re-established soon after disturbance (Marrs et al., 1998; Hughes, 1998a). Atkinson (1989) suggested that trawling was unlikely to affect burrowing megafauna (other than Nephrops) to ‘any great extent’.  Similarly, Vergnon & Blanchard, 2006; OSPAR, 2010) noted that burrowing megafauna (Nephrops and other non-commercial crustaceans) did not show any reduction in total biomass or abundance in highly exploited sites. In their study, Nephrops norvegicus, Munida rugosa and Liocarcinus depurator dominated highly exploited sites in the Bay of Biscay (Vergnon & Blanchard, 2006).

Sensitivity assessment. The burrowing habit of the important characterizing species probably confers some protection from direct impacts of surface abrasion.  Therefore, resistance is assessed as Medium (loss of <25% of individuals) as some individuals may be exposed within the direct footprint when on the surface.  Most Nephrops populations are reported to be resilient to fishing activity and the majority of the population will probably remain to support recovery.  However, there is the potential for overfishing in populations enclosed by hydrology (e.g. in the Irish Sea) or in sea lochs. In addition, while Callianassa subterranea may recover quickly, Calocaris macandreae may take longer to recover due to its benthic larvae and lower fecundity and Maxmuelleria lankesteri is long-lived, with stable populations and low recruitment rates. Therefore, resilience is assessed as Medium, so sensitivity is assessed as Medium.  

Penetration or disturbance of the substratum subsurface

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

Evidence

Species living in deep subtidal mud habitats are considered to be more vulnerable to physical disturbance as they are adapted to stable conditions (Pommer et al., 2016).  In general, species with large body size, low dispersal, late maturation and long lifespan are considered sensitive to physical disturbance (Bolam et al., 2014; Pommer et al., 2016). Similarly, sessile epifauna and species that live at or near the sediment surface are likely to be more vulnerable to physical disturbance than deep-burrowing or mobile species (Pommer et al., 2016). Large bioturbating or bio-irrigating species may be especially sensitive and their loss may affect the community (Widdicombe et al., 2004; Pommer et al., 2016).

Hinz et al. (2009) noted that different studies on the effects of otter trawl disturbance in muddy sediments gave mixed results and that the effect on abundance, biomass and diversity at a community level were largely inconsistent between studies. For example, experimental studies on short-term effects showed modest changes in the benthic communities (e.g. Tuck et al., 1998) and meta-analysis suggested that otter trawling on muddy sediments had one of the least negative impacts on the benthos (Kaiser et al., 2006). However, other studies showed that areas of seabed protected by wrecks from Nephrops trawls had higher abundance and biomass of benthos (Ball et al., 2000), while Smith et al. (2000) showed significantly lower abundance, biomass and species richness of benthos in high-intensity trawling lanes. Hinz et al. (2009)  suggested that the differences in results were the result of differences in statistical analysis, prior fishing intensity and duration of the studies. Hinz et al. (2009) reported that chronic otter trawling from a Nephrops fishery had significant negative effects on the benthic macrofauna. Hinz et al. (2009) concluded that while the initial impact of otter trawl on muddy sediments was modest, the long-term disturbance could lead to profound changes in the benthic communities, especially epifauna and shallow burrowing infauna.

Nephrops norvegicus fisheries could, therefore, affect burrowing megafauna and sea pen biotopes. Nephrops is a commercially targeted species that is harvested by static and mobile gears. Information on the European fisheries for this species is summarised by Ungfors et al. (2013). It is difficult to conduct stock assessments on Nephrops, which can only be harvested selectively by trawls and static gears. Nephrops cannot be aged directly. European Nephrops fisheries are managed as Functional Units (FUs), which are smaller than the usual ICES sub-regions due to the limited dispersal abilities of Nephrops. The estimates of abundance, and hence the recommended maximum sustainable yield (MSY), the related Biomass trigger points and fishing mortality (F_MSY), estimated harvest rates and ICES' recommended limits on landings and by-catch vary between FUs (Ungfors et al., 2013; Marine Scotland, 2016).  For example, harvest rates (ratio of total catch to absolute abundance) vary from ca 5-25% between 2007 and 2015 in the Farn Deeps, to ca 5-30% between 2005 and 2015 in South Minch (Marine Scotland, 2016). Marine Scotland (2016) suggested that the abundance of most stocks in the North Sea has declined to the MSY Biomass trigger point but remained above the F_MSY trigger point. However, in West Scotland, most stocks are above the Biomass trigger point but fluctuate around the F_MSY (Marine Scotland, 2016). Nevertheless, landings of Nephrops in 2014 were 13,700 tonnes in the North Sea and 12,800 in West Scotland (Marine Scotland, 2016).

Nephrops trawls catch specimens that are foraging at the surface. Trawl-caught Nephrops females were reported to have fewer eggs on average than creel-caught females from the same area, during an experimental study, and it was likely that the eggs may be lost due to physical abrasion (Chapman & Ballantyne, 1980). The proportion of eggs lost to abrasion ranged from 11-22% in samples taken from the Clyde and West of Kintyre (Chapman & Ballantyne, 1980).  The entrances to Nephrops burrows are likely to be damaged by abrasion. However, Marrs et al. (1998) reported that burrows were re-established within 2 days providing that the occupant had remained unharmed (Marrs et al., 1998). Nevertheless, burrow density was lower in frequently trawled areas of Loch Fyne except in areas protected from trawling by submarine obstructions (Howson & Davies, 1991; Hughes, 1998a). Video studies have found that only a low proportion (circa 5%) of Nephrops that approached creels to enter them (Bjordal, 1986; Adey, 2007, cited in Ungfors et al., 2013).  Factors that govern emergence will influence catch rates as only individuals that have emerged from burrows will be caught by trawl hauls.  The degree of emergence from burrows for feeding or mating appears to be mainly governed by light intensities and therefore depends on factors such as time of day and season and varies between populations at different depths (Katoh et al., 2013).  Experimental trawling (Bell et al., 2008) to evaluate catch rates showed that catchability varied between vessels in the same area and that catch rates were strongly linked to tidal cycles with increased catch rates at spring rather than neap tides. Catch rates differ between genders (Ungfors et al., 2013); berried females tend to stay within burrows and are rarely caught in trawls (Aguzzi and Sarda 2008, cited in Katoh et al., 2013). The population of Nephrops in the Irish Sea, in muds between the Isle of Man and the Irish coast, may be an exception.  The area is subject to a near-surface gyre that retains larvae in the vicinity of the adults, so that while the population is self-sustaining, it may be vulnerable to over-exploitation as it is unlikely to receive recruitment from the surrounding area (Hill et al., 1996b, 1997b; Hughes, 1998a).  Hughes (1998a) noted that areas that were unsuitable for trawling due to rocky outcrops or other obstacles were often exploited by creeling. Hughes (1998a) suggested that trawling could reduce the density of Nephrops in confined sea lochs but cited Atkinson’s observation that the resilience of Nephrops populations to trawling is enhanced by the fact that juveniles and egg-bearing females remain in their burrows and are not caught by trawls.

Calocaris macandreae is suggested to rarely venture onto the surface (Nash et al. 1984).  Bergmann et al. (2002) noted that small numbers of Calocaris macandreae were by-catch in Nephrops trawls in the Clyde Sea. Comparisons between grab samples collected at trawled and untrawled sites in the Oslofjord, a northern branch of the Skagerrak in the North Sea, showed that Calocaris macandreae were depleted at trawled sites.  The mean abundance of Calocaris macandreae was 41.5 individuals per m² (ca ±9.91) in non-trawled areas and 14.5 individuals per m² (ci.±4.99) in trawled areas (Olsgard et al., 2008).  Trawled areas were visited by otter trawlers targeting Pandalus montagui between 50 and 100 times per year, and based on the size of the trawls and the boat speed, each part of these areas is trawled on average 2–3 times per year (Olsgard et al., 2008).  It is not clear whether the impact is cumulative with decreases in the population occurring incrementally or if the first pass removes the most vulnerable individuals, and those that remain are either new recruits or individuals that are more resistant due to factors such as burrow depth. However, Pommer et al. (2016) did not find a significant difference in the abundance of Calocaris macandreae with trawling intensity in the Kattegat. Duineveld et al. (2007) reported a higher species diversity and abundance of mud shrimps (Callianassa subterranea and Upogebia deltura) with a fisheries exclusion zone in the North Sea than in the surrounding area.

Bolam et al. (2014) suggested that spoon worms (Echiura) of the family Bonellidae (the family to which Maxmuelleria lankesteri belongs) had a high sensitivity to trawling based on their average sensitivity score from eight traits, and high scores for body size, morphology, lack of mobility, longevity and low recruitment, in their biological traits analysis. However, the depth of the burrows constructed by characterizing megafauna (mud-shrimps and Maxmuelleria lankesteri) probably protects the species from surface abrasion and fishing activities. For example, Callianassa subterranea creates a complex lattice of galleries at 30-40 cm below the surface in the fine muds but burrows less deeply (9-23 cm) in coarse sediments (Rowden & Jones, 1995; Hughes, 1998a).  Calocaris macandreae creates burrows with a total depth of 21 cm in muddy sediments with a high silt content (Buchanan, 1963; Hughes, 1998a); Maxmuelleria lankesteri burrows up to 80 cm into the sediment (Nickell et al., 1995; Hughes, 1998a); and Nephrops norvegicus burrows to 20-30 cm and is found in soft mud sediments (Rice and Chapman 1971; Nash et al. 1984; Hughes, 1998a). Based on burrow depths (maximum depth 21 cm for Calocaris macandreae, 30 cm for Nephrops norvegicus and up to 80 cm for Maxmuelleria lankesteri ) the potential effect of penetrative gear will depend on the depth to which the gear penetrates the substratum and, hence, gear type. 

The burrow opening may be damaged (as above) but observations from Loch Sween suggest that they are re-established soon after disturbance (Marrs et al., 1998; Hughes, 1998a). Atkinson (1989) suggested that trawling was unlikely to affect burrowing megafauna (other than Nephrops) to ‘any great extent’.  Similarly, Vergnon & Blanchard, 2006; OSPAR, 2010) noted that burrowing megafauna (Nephrops and other non-commercial crustaceans) did not show any reduction in total biomass or abundance in highly exploited sites. In their study, Nephrops norvegicus, Munida rugosa and Liocarcinus depurator dominated highly exploited sites in the Bay of Biscay (Vergnon & Blanchard, 2006).

Sensitivity assessment. The burrowing habit of the important characterizing species probably confers some protection from direct impacts depending on the depth of penetration of the passing fishing gear or other penetrative activity.  Penetration of the substratum surface may damage the proboscis of Maxmuelleria lankesteri but more importantly remove shallow burrowed specimens of the burrowing megafauna, especially juveniles, and disturb and damage the burrow network within the sediment. Therefore, resistance is assessed as Low (loss of 25%-75% of individuals) as some individuals may be exposed within the direct footprint on the surface or in shallow parts of their burrows.  Most Nephrops populations are reported to be resilient to fishing activity and the majority of the population will probably remain to support recovery.  However, there is the potential for overfishing in populations enclosed by hydrology (e.g. in the Irish Sea) or in sea lochs. In addition, while Callianassa subterranea may recover quickly, Calocaris macandreae may take longer to recover due to its benthic larvae and lower fecundity and Maxmuelleria lankesteri may take a long time to recover due to its low recruitment potential. Therefore, resilience is assessed as Low and sensitivity is assessed as High.  

Changes in suspended solids (water clarity)

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

Evidence

The eye of Nephrops norvegicus is well adapted to low levels of light at the sea bed and hence changes in clarity are unlikely to interfere with visual perception. Nephrops norvegicus emerge from burrows and, due to adaptations to ambient light, Nephrops in shallower waters emerge from burrows at dawn and dusk, whereas those from deeper waters emerge about midday (Ball et al., 2000b).  Alteration in light intensity due to turbidity may, therefore, alter emergence rhythms.  Aréchiga & Atkinson (1975) reported that the burrowing activity of Nephrops norvegicus is restricted to an optimum range of light intensity from about 10,000 to 10 m-c (meter/candles) (equivalent to approximately, 10% to 0.001% of natural daylight).  

Calocaris macandreae are considered to rarely emerge from the burrow system and to mostly feed on organic material within the burrow deposits. Callianassa subterranea also feeds on the organic matter within its burrow. Maxmuelleria lankesteri does not leave its burrow but extends its proboscis to the surface to feed, and is thought to be highly adverse to light (Hughes, 1998a).  

Sensitivity assessment.  The biotope occurs in sheltered areas, in fine sediments, and subject to high suspended sediment loads. Therefore, the important characteristic species are unlikely to be impacted by an increase in suspended sediments.  As they dwell in deep burrows (and only emerge for short periods of time, e.g. Nephrops) they are unlikely to be affected by the resultant increase in turbidity and reduction in light. Resistance is, therefore, assessed as High based on its burrowing habit and resilience is High (based on no impact to recover from) and the biotope is 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 important characteristic burrowing megafauna (mud-shrimp and Nephrops) are unlikely to be affected adversely as they are active burrowers and Nephrops norvegicus, Calocaris macandreae and Callianassa subterranea were reported within the Garroch Head (Firth of Clyde) sludge dumping ground (Smith, 1988; cited in Hughes, 1998a).  In addition, if the deposited sediment occludes burrow openings, then they would be reopened quickly. Observations from Loch Sween suggest that they are re-established soon after experimental disturbance (Hughes, 1998a).

This biotope occurs in deep, sheltered muddy habitats where the accretion rates are potentially high. It is probable therefore that deposition of 5 cm of fine sediment will have little effect other than to temporarily suspend feeding and the energetic cost of burrowing. Therefore, a resistance of High is suggested, resulting in a resilience of High and sensitivity of Not sensitive.  

Smothering and siltation rate changes (heavy)

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

Evidence

The important characteristic burrowing megafauna (mud-shrimp and Nephrops) are unlikely to be affected adversely as they are active burrowers and Nephrops norvegicus, Calocaris macandreae and Callianassa subterranea were reported within the Garroch Head (Firth of Clyde) sludge dumping ground (Smith, 1988; cited in Hughes, 1998a).  In addition, if the deposited sediment occludes burrow openings, then they would be reopened quickly. Observations from Loch Sween suggest that they are re-established soon after experimental disturbance (Hughes, 1998a).

This biotope occurs in deep, sheltered muddy habitats where the accretion rates are potentially high. It is probable therefore that deposition of 30 cm of fine sediment will have little effect other than to temporarily suspend feeding and the energetic cost of burrowing. Therefore, a resistance of High is suggested, resulting in a resilience of High and sensitivity of Not sensitive.  

Litter

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

Evidence

Not assessed.

Electromagnetic changes

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

Evidence

No evidence 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

Some of the characterizing species associated with this biotope, in particular, the sea pens, may respond to sound vibrations and can withdraw into the sediment. Feeding will resume once the disturbing factor has passed. However, most of the species are infaunal and unlikely respond to noise disturbance at the benchmark level. Therefore, this pressure is probably Not relevant in this biotope.

Introduction of light or shading

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

Evidence

Nephrops norvegicus emerge from burrows and, due to adaptations to ambient light, Nephrops in shallower waters emerge from burrows at dawn and dusk, whereas those from deeper waters emerge about midday (Ball et al., 2000b).  Alteration in light intensity due to turbidity may, therefore, alter emergence rhythms.  Aréchiga & Atkinson (1975) reported that the burrowing activity of Nephrops norvegicus is restricted to an optimum range of light intensity from about 10,000 to 10 m-c (meter/candles) (equivalent to approximately, 10% to 0.001% of natural daylight). But Nephrops are more active by day in deeper waters (ca 100 m) (Hughes, 1998a). In the shallow waters of Loch Sween, Maxmuelleria lankesteri only extends its proboscis to the surface to feed at night, and then only for short periods (Hughes et al., 1993). Hughes (1998a) this species would behave differently in deep water. Calocaris macandreae is considered to rarely emerge from its burrow system (Hughes, 1998a).

Sensitivity assessment. Light is probably not relevant in the deep examples of this biotope. In shallow examples of the biotope, shading may increase the time available for feeding by Nephrops or Maxmuelleria lankesteri, while an increase in ambient light might decrease feeding. Therefore, a resistance of High is recorded. Resilience is High (by default) so that the biotope is probably Not sensitive at the benchmark level.

Barrier to species movement

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

Evidence

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

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

Most species within the biotope are burrowing and have no or poor visual perception and are unlikely to be affected by visual disturbance such as shading. Epifauna such as crabs have well developed visual acuity and are likely to respond to movement in order to avoid predators. However, it is unlikely that the species will be affected by visual disturbance at the benchmark level.

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

No evidence of genetic modification, breeding, or translocation in sea pens or burrowing megafauna was found.

Introduction or spread of invasive non-indigenous species

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

Evidence

Sternapsis scutata is a non-native polychaete that has extended its range in inshore muddy sediments in the south-west of the UK (Shelley et al., 2008). However, in mesocosm experiments, little effect on biological functioning was detected after the introduction of the polychaete and a doubling of its biomass (Shelley et al., 2008). The red king crab Paralithodes camtschaticus is a voracious, omnivorous benthic predator that has spread from the Barents Sea to the coast of Norway, where it is a threat to shellfisheries and demersal fisheries. It has not been recorded in UK waters to date (GBNNSIP, 2011).

No direct evidence of the effect of non-native species on sea pen and burrowing megafauna communities was found. However, this assessment should be revisited in light of new evidence.

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

The infection of Nephrops norvegicus by a parasitic dinoflagellate of the genus Hematodinium has been known since the mid-1980s (Field et al., 1992). Infected populations have been found in the Irish Sea, Scottish sites in the Clyde Sea area and the west and east coasts. Hematodinium has also been reported in Nephrops in the German Bight, the Skagerrak and Kattegat (Briggs & McAliskey, 2002). Infected animals are recognized by an opaque vivid body colouration, believed to be due to high densities of parasites in the haemolymph. The muscle of infected animals is said to have a bitter taste. The infection causes a general morbidity of the lobster and a reduction in swimming performance. Death usually occurs when the parasite bursts out of the haemolymph (Marrs, pers. comm.). Recovery of Hematodinium infected Nephrops has not been observed to date (Stentiford et al., 2001). Results from the Irish Sea and Scottish surveys show a seasonal pattern to the level of Hematodinium infection in Nephrops norvegicus, with peaks in spring (Stentiford et al., 2001; Briggs & McAliskey, 2002). There was also a marked spatial variability in infection rates in animals in the Irish Sea (Briggs & McAliskey, 2002). The prevalence of infection is higher in immature animals although the reasons for this are still unclear. High mortalities seen during some surveys although these values may be an artefact brought about by the increased catchability of infected Nephrops as swimming performance falls with the severity of infection (Stentiford et al., 2000). This may lead to overestimation of the actual prevalence of infection in fishing stocks. Briggs & McAliskey (2002) report that the disease has been present in populations of Nephrops at least since 1994 and despite inflicting juvenile mortality on the Nephrops stock, recent assessments indicated a stable situation.

Mud shrimp are parasitized by parasitic isopods called bopyrids. The parasite lives in the gills and reduces reproductive output (Hughes, 1998a). Rowden & Jones (1994) reported that 11% of Callianassa subterranea in the southern North Sea were infected.  Other than a reduction in reproduction, no other effects were reported (Hughes, 1998a).

Sensitivity assessment. As Hematodinium could result in increased mortality in Nephrops, a resistance of Medium is recorded. Resilience is probably Medium so that the sensitivity of the biotope is assessed as Medium.

Removal of target species

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

Evidence

Species living in deep subtidal mud habitats are considered to be more vulnerable to physical disturbance as they are adapted to stable conditions (Pommer et al., 2016).  In general, species with a large body size, low dispersal, late maturation and long lifespan are considered sensitive to physical disturbance (Bolam et al., 2014; Pommer et al., 2016). Similarly, sessile epifauna and species that live at or near the sediment surface are likely to be more vulnerable to physical disturbance than deep-burrowing or mobile species (Pommer et al., 2016). Large bioturbating or bio-irrigating species may be especially sensitive and their loss may affect the community (Widdicombe et al., 2004; Pommer et al., 2016).

Hinz et al. (2009) noted that different studies on the effects of otter trawl disturbance in muddy sediments gave mixed results and that the effect on abundance, biomass and diversity at a community level were largely inconsistent between studies. For example, experimental studies on short-term effects showed modest changes in the benthic communities (e.g. Tuck et al., 1998) and meta-analysis suggested that otter trawling on muddy sediments had one of the least negative impacts on the benthos (Kaiser et al., 2006). However, other studies showed that areas of seabed protected by wrecks from Nephrops trawls had higher abundance and biomass of benthos (Ball et al., 2000), while Smith et al. (2000) showed significantly lower abundance, biomass and species richness of benthos in high-intensity trawling lanes. Hinz et al. (2009)  suggested that the differences in results were the result of differences in statistical analysis, prior fishing intensity and duration of the studies. Hinz et al. (2009) reported that chronic otter trawling from a Nephrops fishery had significant negative effects on the benthic macrofauna. Hinz et al. (2009) concluded that while the initial impact of otter trawl on muddy sediments was modest, the long-term disturbance could lead to profound changes in the benthic communities, especially epifauna and shallow burrowing infauna.

Nephrops norvegicus fisheries could, therefore, affect burrowing megafauna and sea pen biotopes. Nephrops is a commercially targeted species that is harvested by static and mobile gears. Information on the European fisheries for this species is summarised by Ungfors et al. (2013). It is difficult to conduct stock assessments on Nephrops, which can only be harvested selectively by trawls and static gears. Nephrops cannot be aged directly. European Nephrops fisheries are managed as Functional Units (FUs), which are smaller than the usual ICES sub-regions due to the limited dispersal abilities of Nephrops. The estimates of abundance, and hence the recommended maximum sustainable yield (MSY), the related Biomass trigger points and fishing mortality (F_MSY), estimated harvest rates and ICES' recommended limits on landings and by-catch vary between FUs, (Ungfors et al., 2013; Marine Scotland, 2016).  For example, harvest rates (ratio of total catch to absolute abundance) vary from ca 5-25% between 2007 and 2015 in the Farn Deeps, to ca 5-30% between 2005 and 2015 in South Minch (Marine Scotland, 2016). Marine Scotland (2016) suggest that the abundance of most stocks in the North Sea has declined to MSY Biomass trigger point but remain above the F_MSY trigger point. However, in West Scotland, most stocks are above the Biomass trigger point but fluctuate around the F_MSY (Marine Scotland, 2016). Nevertheless, landings of Nephrops in 2014 were 13,700 tonnes in the North Sea and 12,800 in West Scotland (Marine Scotland, 2016).

Nephrops trawls catch specimens that are foraging at the surface. Trawl caught Nephrops females were reported to have fewer eggs on average than creel caught females from the same area, during an experimental study, and that it was likely that the eggs may be lost due to physical abrasion (Chapman & Ballantyne, 1980). The proportion of eggs lost to abrasion ranged from 11-22% in samples taken from the Clyde and West of Kintyre (Chapman & Ballantyne, 1980).  The entrances to Nephrops burrows are likely to be damaged by abrasion. However, Marrs et al. (1998) reported that burrows were re-established within 2 days providing that the occupant had remained unharmed (Marrs et al., 1998). Nevertheless, burrow density was lower in frequently trawled areas of Loch Fyne except in areas protected from trawling by submarine obstructions (Howson & Davies, 1991; Hughes, 1998a). Video studies have found that only a low proportion (circa 5%) of Nephrops that approached creels enter them (Bjordal, 1986; Adey, 2007, cited in Ungfors et al., 2013).  Factors that govern emergence will influence catch rates as only individuals that have emerged from burrows will be caught by trawl hauls.  The degree of emergence from burrows for feeding or mating appears to be mainly governed by light intensities and therefore depends on factors such as time of day and season and varies between populations at different depths (Katoh et al., 2013).  Experimental trawling (Bell et al., 2008) to evaluate catch rates showed that catchability varied between vessels in the same area and that catch rates were strongly linked to tidal cycles with increased catch rates at spring rather than neap tides. Catch rates differ between genders (Ungfors et al., 2013); berried females tend to stay within burrows and are rarely caught in trawls (Aguzzi & Sarda 2008, cited in Katoh et al., 2013). The population of Nephrops in the Irish Sea, in muds between the Isle of Man and the Irish coast, may be an exception. The area is subject to a near-surface gyre that retains larvae in the vicinity of the adults, so that while the population is self-sustaining, it may be vulnerable to over-exploitation as it is unlikely to receive recruitment from the surrounding area (Hill et al., 1996b, 1997b; Hughes, 1998a).  Hughes (1998a) noted that areas that were unsuitable for trawling due to rocky outcrops or other obstacles were often exploited by creeling. Hughes (1998a) suggested that trawling could reduce the density of Nephrops in confined sea lochs but cited Atkinson’s observation that the resilience of Nephrops populations to trawling is enhanced by the fact that juveniles and egg-bearing females remain in their burrows and are not caught by trawls.

Hughes (1998a) suggested that the mix of megafaunal burrowers creates a continuously shifting mosaic of habitat patches that reflected different disturbance.  He suggested that this ‘patchiness’ was a factor in the maintenance of the species diversity of these communities. Although the burrows of different megafaunal burrowers often interconnected, there was no evidence of any relationship between the species, and that the connections were probably accidental. In addition, there was no evidence that any single species of megafaunal burrower was dominant or determined the structure or functioning of the community (Hughes, 1998a).

Sensitivity assessment. The physical effects of Nephrops fisheries are discussed under the ‘abrasion’ and penetration’ pressures above.  However, there is no evidence to suggest that the targeted removal of Nephrops from the community would have any biological effect on the community.  This conclusion is supported by Atkinson’s (1989) observation that trawling was unlikely to affect other megafaunal burrowers to ‘any great extent’.  Similarly, Vergnon & Blanchard, 2006; OSPAR, 2010) noted that burrowing megafauna (Nephrops and other non-commercial crustaceans) did not show any reduction in total biomass or abundance in highly exploited sites. In their study, Nephrops norvegicus, Munida rugosa and Liocarcinus depurator dominated highly exploited sites in the Bay of Biscay (Vergnon & Blanchard, 2006).  In mesocosm experiments, Widdicombe et al. (2004) noted that bioturbation of muddy sediments associated by burrow formation (by Calocaris macandreae) was less important for maintaining biodiversity than the bioturbation of bulldozing species (e.g. Brissopsis lyrifera and Aphrodita aculeata) in the surface 10 cm of the sediment.  In addition, Sciberras et al., (2016) concluded that the physical effects of trawling on the biogeochemistry of muds were larger than in sands but that these changes were not mediated by changes in the infauna. Therefore, a resistance of High is recorded, so that resilience is also High (by default) and the biotope is recorded as Not sensitive.

Removal of non-target species

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

Evidence

The physical effects of fisheries are discussed under the ‘abrasion’ and 'penetration’ pressures above.  Species living in deep subtidal mud habitats are considered to be more vulnerable to physical disturbance as they are adapted to stable conditions (Pommer et al., 2016).  In general, species with large body size, low dispersal, late maturation and long lifespan are considered sensitive to physical disturbance (Bolam et al., 2014; Pommer et al., 2016). Similarly, sessile epifauna and species that live at or near the sediment surface are likely to be more vulnerable to physical disturbance than deep-burrowing or mobile species (Pommer et al., 2016). Large bioturbating or bio-irrigating species may be especially sensitive and their loss may affect the community (Widdicombe et al., 2004; Pommer et al., 2016).

Hinz et al. (2009) noted that different studies on the effects of otter trawl disturbance in muddy sediments gave mixed results and that the effect on abundance, biomass and diversity at a community level were largely inconsistent between studies. For example, experimental studies on short-term effects showed modest changes in the benthic communities (e.g. Tuck et al., 1998) and meta-analysis suggested that otter trawling on muddy sediments had one of the least negative impacts on the benthos (Kaiser et al., 2006). However, other studies showed that areas of seabed protected by wrecks from Nephrops trawls had higher abundance and biomass of benthos (Ball et al., 2000), while Smith et al. (2000) showed significantly lower abundance, biomass and species richness of benthos in high-intensity trawling lanes. Hinz et al. (2009)  suggested that the differences in results were the result of differences in statistical analysis, prior fishing intensity and duration of the studies. Hinz et al. (2009) reported that chronic otter trawling from a Nephrops fishery had significant negative effects on the benthic macrofauna. Hinz et al. (2009) concluded that while the initial impact of otter trawl on muddy sediments was modest, the long-term disturbance could lead to profound changes in the benthic communities, especially epifauna and shallow burrowing infauna.

However, there is no evidence to suggest that the targeted removal of Nephrops or other megafaunal burrowers from the community would have any biological effect on the community.  This conclusion is supported by Atkinson’s (1989) observation that trawling was unlikely to affect other megafaunal burrowers to ‘any great extent’.  Similarly, Vergnon & Blanchard (2006; OSPAR, 2010) noted that burrowing megafauna (Nephrops and other non-commercial crustaceans) did not show any reduction in total biomass or abundance in highly exploited sites. In their study, Nephrops norvegicus, Munida rugosa and Liocarcinus depurator dominated highly exploited sites in the Bay of Biscay (Vergnon & Blanchard, 2006).  In mesocosm experiments, Widdicombe et al. (2004) noted that bioturbation of muddy sediments associated with burrow formation (by Calocaris macandreae) was less important for maintaining diversity than the bioturbation of bulldozing species (e.g. Brissopsis lyrifera and Aphrodita aculeata) in the surface 10 cm of the sediment.  In addition, Sciberras et al. (2016) concluded that the physical effects of trawling on the biogeochemistry of muds were larger than in sands but that these changes were not mediated by changes in the infauna. 

Hughes (1998) suggested that the mix of megafaunal burrowers creates a continuously shifting mosaic of habitat patches that reflected different disturbances.  He suggested that this ‘patchiness’ was a factor in the maintenance of the species diversity of these communities. Although the burrows of different megafaunal burrowers are often interconnected, there was no evidence of any relationship between the species, and the connections were probably accidental. In addition, there was no evidence that any single species of megafaunal burrower was dominant or determined the structure or functioning of the community (Hughes, 1998).  Therefore, a resistance of 'High' is recorded, so that resilience is also 'High' (by default) and the biotope is recorded as 'Not sensitive'.