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

Kain (1964) reported that Laminaria hyperborea sporophyte growth and reproduction could occur within a temperature range of 0°C and 20°C. Upper and lower lethal temperatures have been estimated at between 1-2°C above or below the extremes of this range (Birkett et al., 1998b). Above 17°C gamete survival is reduced (Kain, 1964, 1971) and gametogenesis is inhibited at 21°C (Dieck, 1992). It is, therefore, likely that Laminaria hyperborea recruitment will be impaired at a sustained temperature increase of above 17°C. Sporophytes, however, can tolerate slightly higher temperatures of 20°C. Temperature tolerances for Laminaria hyperborea also vary seasonally and temperature changes are less tolerated in winter months than summer months (Birkett et al., 1998b). However, it has a wide distribution in the North East Atlantic from Iceland south to the Bay of Biscay and Portugal. 

Subtidal red algae are less tolerant of temperature extremes than intertidal red algae, surviving between -2°C and 18-23°C (Lüning 1990; Kain & Norton, 1990).  A temperature increase may affect growth, recruitment or interfere with reproduction processes. For example, there is some evidence to suggest that blade growth in Delesseria sanguinea is delayed until ambient sea temperatures fall below 13°C. Blade growth is also likely to be intrinsically linked to gametangia development (Kain, 1987) and maintenance of sea temperatures above 13°C may affect recruitment success.

No empirical evidence was found for the temperature tolerance of Sabellaria spinulosa.  Nevertheless, its widespread distribution suggests that it is tolerant of temperature variation (Gibb et al., 2014). Sabellaria spinulosa has the greatest geographical range of all the sabellariids, according to current records, encompassing Iceland, the Skagerrak and the Kattegat, the North Sea, the English Channel, the northeast Atlantic, the Mediterranean, the Wadden Sea and the Indian Ocean, (Achari, 1974; Riesen & Reise, 1982; Reise & Schubert,1987; Hayward & Ryland, 1998; Foster-Smith, 2000; Collins, 2005). The associated epifauna are highly variable and reflect the assemblages found in adjacent biotopes. 

Sensitivity assessment. In the UK, northern to southern Sea Surface Temperature (SST) ranges from 8-16°C in summer and 6-13°C in winter (Beszczynska-Möller & Dye, 2013). Overall, a chronic change (2°C for a year) outside the normal range for a year may reduce recruitment and growth, resulting in a minor loss in the population of kelp, especially in winter months or in southern examples of the biotope, although Sabellaria crusts are probably resistant.  However, an acute change (5°C for a month; e.g. from thermal effluent) may result in loss of abundance of kelp or extent of the bed, especially in winter. Therefore, resistance to the pressure is assessed as 'Medium' and resilience as  'Medium' so that the sensitivity of this biotope to increases in temperature is assessed as 'Medium'.

Temperature decrease (local)

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

Evidence

Kain (1964) reported that Laminaria hyperborea sporophyte growth and reproduction could occur within a temperature range of 0°C and 20°C. Upper and lower lethal temperatures have been estimated at between 1-2°C above or below the extremes of this range (Birkett et al., 1998b). Subtidal red algae can survive at temperatures between -2°C and 18-23°C (Lüning, 1990; Kain & Norton, 1990). Laminaria hyperborea is a boreal northern species with a geographic range from mid-Portugal to Northern Norway (Birket et al., 1998b), and a mid-range within southern Norway (60°-65° North)(Kain, 1971). The average seawater temperature for southern Norway in October is 12-13°C (Miller et al., 2009).  Also, the average annual sea temperature, from 1970 to 2014, was 8°C (Beszczynska-Möller & Dye, 2013). The available information suggests that Laminaria hyperborea forest and canopy would not be affected by a decrease in sea temperature at the benchmark level.

Sabellaria spinulosa occurs north to the Arctic and is, therefore, probably tolerant of a decrease in temperature at the pressure benchmark. This conclusion is supported by observations that Sabellaria spinulosa appeared unaffected by the cold, on oyster grounds in the River Crouch, throughout the severe winter of 1962–1963 The mean daily temperature was recorded at a depth of one fathom (1.8 m) below low water (equinoctial spring tide) and the lowest temperature recorded was -1.8°C (Crisp, 1964). At Penmon in Bangor, Sabellaria spinulosa also did not to suffer from the low temperatures and live individuals were found readily (Crisp, 1964). 

Sensitivity assessment. Therefore, the evidence suggests that neither the Laminaria hyperborea canopy nor the Sabellaria crusts would be adversely affected by a decrease in temperature at the benchmark level. Therefore, resistance to the pressure is assessed as ‘High’ and resilience as ‘High’ so that the sensitivity of this biotope to a decrease in temperature 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

Lüning (1990) suggested that 'kelps' were stenohaline and that their general tolerance to salinity as a phenotypic group covered 16-50 psu over a 24 hr period. Optimal growth probably occurs between 30-35 psu ('Full' salinity) and growth rates are likely to be affected by periodic salinity stress. Birkett et al. (1998b) suggested that long-term increases in salinity may affect Laminaria hyperborea growth and may result in loss of affected kelp and, therefore, loss of the biotope. No evidence for the physiological tolerance of Sabellaria spinulosa to salinity change was found by Gibb et al. (2014).  Roberts et al. (2010b) reported that hypersaline effluents from desalination plants disperse with tens of metres of the discharge point but reported widespread alteration in seagrass and soft sediment communities in poorly flushed environments. Hypersaline effluents are likely to sink to the seabed, and potentially penetrate the sediment. However, the water movement characteristic of this biotope is likely to disperse the effluent and limit the effect to the immediate vicinity of any discharge point.

Sensitivity assessment. The evidence suggests that the Laminaria hyperborea canopy might be affected by hypersaline conditions. Therefore, a precautionary resistance assessment of 'Medium' is suggested but with Low confidence. Resilience is probably 'Medium' so that sensitivity is assessed as 'Medium'.

Salinity decrease (local)

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

Evidence

Lüning (1990) suggested that 'kelps' were stenohaline and that their general tolerance to salinity as a phenotypic group covered 16-50 psu over a 24 hr period. Optimal growth probably occurs between 30-35 psu ('Full' salinity) and growth rates are likely to be affected by periodic salinity stress. Birkett et al. (1998b) suggest that long-term changes in salinity may result in loss of affected kelp and, therefore, loss of this biotope.

Hopkin & Kain (1978) tested Laminaria hyperborea sporophyte growth at various low salinity treatments. The results showed that Laminaria hyperborea sporophytes could grow 'normally' at 19 psu, but that growth was reduced at 16 psu and sporophytes did not grow at 7 psu. A decrease in one MNCR salinity scale from 'Full' salinity (30-40 psu) to 'Reduced' salinity (18-30 psu) could result in a decrease of Laminaria hyperborea sporophyte growth. Laminaria hyperborea may also be out-competed by low salinity tolerant species e.g. Saccharina latissima (Karsten, 2007), or the Invasive Non-Indigenous Species Undaria pinnatifida (Burrows et al., 2014).  If salinity was returned to 'Full' salinity (30-40 psu) Laminaria hyperborea could out-compete Saccharina latissima and re-establish community dominance in 2-4 years (Kain, 1975; Leinaas & Christie, 1996), however full habitat structure may take over 10 years to recover (Birkett et al., 1998b; Christie et al., 1998). The ability of Laminaria hyperborea to out-compete Undaria pinnatifida within the UK is, however, unknown (Heiser et al., 2014), and any interspecific interaction between Laminaria hyperborea and Undaria pinnatifida is not included within this sensitivity assessment.

No evidence for the physiological tolerances of Sabellaria spinulosa to decreases in salinity was found by Gibb et al. (2014).  Sabellaria spinulosa does not seem to occur in very low salinity areas (Holt et al.,1998) but has been recorded from estuaries including the Crouch, Mersey (Killeen & Light, 2000) and the Thames (Limpenny, 2010).  Buhs & Reise (1997) surveyed 12 channel systems in the Wadden Sea and found that Sabellaria spinulosa reefs occurred in the northern tidal inlets that experienced salinity levels ranging from 28 to 30 psu.  There is some speculation (Foster-Smith & Hendrick, 2003) that Mcintosh (1922) misidentified samples of Sabellaria spinulosa as the congener Sabellaria alveolata from the Humber estuarine population (Holt et al., 1998).  These records indicate that reduced and variable salinities can be tolerated to some extent but the paucity of records suggests that areas of reduced salinity do not provide optimal habitat. 

Sensitivity assessment. Therefore a reduction in salinity from 'Full' (30-35) to 'Reduced' (18-30) for a year, may result in loss of a proportion of the kelp bed, as sporophyte growth is reduced and loss by wave action and herbivory increases, or via competion with opportunistic, low salinity tolerant, species such as Saccharina latissima. Similarly, Sabellaria may not be able to tolerate low salinities, although the evidence is unclear. Therefore, resistance to the pressure is assessed as ‘Low’, and resilience ‘Medium’ so that the sensitivity of this biotope to decreases in salinity is 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

Kregting et al. (2013) measured Laminaria hyperborea blade growth and stipe elongation from an exposed and a sheltered site in Strangford Lough, Ireland, from March 2009 to April 2010. Maximal significant wave height (Hm0) was 3.67 & 2 m and maximal water velocity (Velrms) was 0.6 & 0.3 m/s at the exposed and sheltered sites respectively. Despite the differences in wave exposure and water velocity, there was no significant difference in Laminaria hyperborea growth between the exposed and sheltered sites. Therefore, water flow was found to have no significant effect on Laminaria hyperborea growth at the observed range of water velocities. Biotope structure is, however, different between wave exposed and sheltered sites. Pedersen et al. (2012) observed Laminaria hyperborea biomass, productivity and density increased with an increase in wave exposure. At low wave exposure, Laminaria hyperborea canopy-forming plants were smaller, had lower densities and had higher mortality rates than at exposed sites. At low wave exposure, Pedersen et al. (2012) suggested that high epiphytic loading on Laminaria hyperborea impaired light conditions, nutrient uptake, and increased the drag on the host Laminaria hyperborea during extreme storm events.

The morphology of the stipe and blade of kelps varies with water flow.  In wave exposed areas, for example, Laminaria hyperborea develops a long and flexible stipe and this is probably a functional adaptation to strong water movement (Sjøtun, 1998). In addition, the lamina becomes narrower and thinner in strong currents (Sjøtun & Fredriksen, 1995). However, the stipe of Laminaria hyperborea is relatively stiff and can snap in strong currents. Laminaria hyperborea is usually absent from areas of high wave action or strong currents, although it is found in the Menai Strait, Wales, where tidal velocities can exceed 4 m/s (NBN, 2015) and in tidal rapids in Norway (J. Jones, pers. comm.).  Laminaria hyperborea growth can persist in very strong tidal streams (>3 m/s). Increased water flow rate may also remove or inhibit grazers including Patella pellucida and Echinus esculentus and remove epiphytic algae growth (Pedersen et al., 2012). The associated algal flora and suspension-feeding faunal populations change significantly with different water flow regimes. Increased water flow rates may reduce the understorey epiflora, to be replaced by an epifauna dominated community (e.g. sponges, anemones and polyclinid ascidians) as in the biotope IR.HIR.KFaR.LhypFa. The composition of the holdfast fauna may also change, e.g. energetic or sheltered water movements favour different species of amphipods (Moore, 1985).

Sabellaria spinulosa tends to occur in areas of high water movement where larvae, tube building materials and food particles are suspended and transported (Jones et al., 2000).  The relative importance of tidal versus wave induced movements to support reefs is, however, unclear (Holt et al., 1998). There is limited in-situ data on the specific water flow tolerances of Sabellaria spinulosa, although colonies have been found in areas with sedimentary bed forms that suggest current velocities in the range of 0.5 m/s to 1.0 m/s (Mistakidis, 1956; Jones et al., 2000; Davies et al., 2009).  In the southern North Sea close to the coast of England, Sabellaria spinulosa reefs have been recorded in areas exposed to peak spring tidal flows of 1.0 m/s (Pearce et al., 2014). Davies et al. (2009) also found, through laboratory experiments with Sabellaria spinulosa in tanks, that increasing the water flow to an average of 0.03 m/s is adequate to begin distribution of the sediment rain from the airlift throughout the tank and that doubling the water flow to almost 0.07 m/s further improved particle distribution throughout the tank.  Therefore, it is likely that Sabellaria spinulosa requires habitats with a water flow above 0.07 m/s so that particles are suspended and distributed for the use of tube building and feeding. 

Tillin (2010) used logistic regression to develop statistical models that indicate how the probability of occurrence of the congener Sabellaria alveolata changes over environmental gradients within the Severn Estuary.  The model predicted response surfaces were derived for each biotope for each of the selected habitat variables, using logistic regression.  From these response surfaces the optimum habitat range for each biotope could be defined based on the range of each environmental variable where the probability of occurrence, divided by the maximum probability of occurrence, is 0.75 or higher.  These results identify the range for each significant variable where the habitat is most likely to occur.  The modelled ranges should be interpreted with caution and apply to the Severn Estuary alone (which experiences large tidal ranges, high currents and extremely high suspended sediment loads and is therefore distinct from many other estuarine systems).  However, these ranges do provide some useful information on environmental tolerances.  The models indicate that for subtidal Sabellaria alveolata the maximum optimal current speed (the range in which it is most likely to occur) ranges from 1.26-2.46 m/s and the optimal mean current speed ranges from 0.5-1.22 m/s.  Although not directly applicable to Sabellaria spinulosa this data suggests that tube-building Sabellariids can occur within a broad range of current speeds. In cases of reduced water flow, Sabellaria spinulosa is likely to suffer a reduction in the supply of suspended food and particles that are integral for growth and repair.  A long-term decrease in water flow may reduce the viability of populations by limiting growth and tube building but no evidence was found for threshold levels relating to impact.

Sensitivity assessment. The IR.MIR.KR.Lhyp and CR.MCR.CSab biotopes and sub-biotopes are characteristic of moderate energy environments due to moderate or greater wave action or strong to weak tidal flow, depending on which source of water movement is dominant in any particular site. This biotope IR.MIR.KR.Lhyp.Sab biotope is found in weak tidal flow but moderate wave exposure, which keeps the sand in suspension.  A significant decrease in water flow might reduce the suspension of sand to the detriment of the Sabellaria crusts but benefit red algae, whereas a significant increase in water flow may increase scour to the detriment of the red algal understorey and possibly kelp recruitment but benefit the Sabellaria spinulosa.  Nevertheless, wave action is the dominant source of water movement in this biotope and a change in peak mean spring bed flow velocity of between 0.1m/s to 0.2m/s for more than 1 year is not likely to affect the structure of the biotope, especially as both kelp and red algal dominated biotopes and Sabellaria crusts occur in moderately strong (0.5-1.5 m/s) and strong water flows (1.5-3 m/s).  Therefore, resistance to the pressure is assessed as ‘High’, and resilience ‘High’ so that the sensitivity of this biotope to changes in water flow is assessed as ‘Not Sensitive’ at the benchmark level.   

Emergence regime changes

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

Evidence

The upper limit of the Laminaria hyperborea bed is determined by wave action, water flow, desiccation, and competition from the more emergence resistant Laminaria digitata. Laminaria hyperborea exposed at extreme low water are very intolerant of desiccation, the most noticeable effect being bleaching of the frond and subsequent death of the meristem and loss of the plant. An increase in wave exposure (see below), as a result of increased emergence, has been found to exclude Laminaria hyperborea from shallow waters due to dislodgement of the sporophyte or snapping of the stipe (Birket et al., 1998b). Hence, an increase in emergence could lead to mortality of exposed Laminaria hyperborea and the associated habitat. However, a decrease in emergence (at the benchmark level) may increase the upper depth restriction of Laminaria hyperborea forest biotope variants. However, limited light availability at depth will decrease the lower extent of Laminaria hyperborea, and may, therefore, result in a shift from forest to park biotope variants at depth. Further increases in depth will cause a community shift to that characterized by circalittoral faunal species, however, this is beyond the scope of the benchmark. Sabellaria spinulosa crusts are most abundant in the subtidal (e.g. CR.MCR.CSab) but crusts can occur in the lower intertidal. 

Sensitivity assessment. Shallow examples of the biotope may lose a proportion of the Laminaria canopy due to an increase in emergence whereas an increase in emergence due to increase water depth might also limit the deeper extents of the Laminaria canopy. Therefore, resistance to the pressure is assessed as ‘Low’, and resilience ‘Medium’ so that the sensitivity of this biotope to changes in emergence is assessed as ‘Medium’.

Wave exposure changes (local)

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

Evidence

Kregting et al. (2013) measured Laminaria hyperborea blade growth and stipe elongation from an exposed and a sheltered site in Strangford Lough, Ireland from March 2009 to April 2010. Wave exposure was found to be between 1.1. to 1.6 times greater between the exposed and sheltered sites. Maximal significant wave height (Hm0) was 3.67 & 2 m and maximal water velocity (Velrms) was 0.6 & 0.3m/s at the exposed and sheltered sites respectively. Despite the differences in wave exposure and water velocity, there was no significant difference in Laminaria hyperborea growth between the exposed and sheltered site.

Biotope structure is, however, different between wave exposed and sheltered sites. Pedersen et al. (2012) observed Laminaria hyperborea biomass, productivity and density increased with an increase in wave exposure. At low wave exposure, Laminaria hyperborea canopy-forming plants were smaller, had lower densities and higher mortality rates than at exposed sites. At low wave exposure, high epiphytic loading on Laminaria hyperborea was theorised to impair light conditions, nutrient uptake, and increase the drag of the host Laminaria hyperborea during extreme storm events.  The morphology of the stipe and blade of kelps vary with water flow. In wave exposed areas, for example, Laminaria hyperborea develops a long and flexible stipe and this is probably a functional adaptation to strong water movement (Sjøtun, 1998). In addition, the lamina becomes narrower and thinner in strong currents (Sjøtun & Fredriksen, 1995). However, the stipe of Laminaria hyperborea is relatively stiff and can snap in strong currents. Laminaria hyperborea is usually absent from areas of extreme wave action and can be replaced by Alaria esculenta. In extreme wave exposures, Alaria esculenta can dominate the shallow sublittoral to a depth of 15 m (Birket et al., 1998b). Increase water flow rate may also remove or inhibit grazers including Patella pellucida and Echinus esculentus and remove epiphytic algae growth (Pedersen et al., 2012). The associated algal flora and suspension-feeding faunal populations change significantly with different water flow regimes. Increased water flow rates may reduce the understorey epiflora, to be replaced by an epifauna dominated community (e.g. sponges, anemones and polyclinid ascidians) as in the biotope IR.HIR.KFaR.LhypFa. The composition of the holdfast fauna may also change, e.g. energetic or sheltered water movements favour different species of amphipods (Moore, 1985).

No direct evidence was found to assess this pressure on Sabellaria spinulosa crusts or reefs. 

Sensitivity assessment. The IR.MIR.KR.Lhyp and CR.MCR.CSab biotopes and sub-biotopes are characteristic of moderate energy environments due to moderate or greater wave action or strong to weak tidal flow, depending on which source of water movement is dominant in any particular site. This biotope IR.MIR.KR.Lhyp.Sab biotope is found in weak tidal flow but moderate wave exposure, which keeps the sand in suspension.  A significant decrease in wave action could reduce the suspension of sand to the detriment of the Sabellaria crusts but benefit red algae, whereas a significant increase in wave action could increase scour to the detriment of the red algal understorey and possibly kelp recruitment but benefit the Sabellaria spinulosa.  Nevertheless, a change in nearshore significant wave height >3% but <5% is unlikely to have a significant effect in areas subject to moderate wave exposure.  Therefore, resistance to the pressure is assessed as ‘High’, and resilience ‘High’ so that the sensitivity of this biotope to changes in water flow is assessed as ‘Not Sensitive’ 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.

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.

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.

Radionuclide contamination

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

Evidence

No evidence

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 but evidence is presented where available.

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

Reduced oxygen concentrations have been shown to inhibiting both photosynthesis and respiration in macroalgae (Kinne, 1977). Despite this, macroalgae are thought to buffer the environmental conditions of low oxygen, thereby acting as a refuge for organisms in oxygen-depleted regions especially if the oxygen depletion is short-term (Frieder et al., 2012).  Rapid recovery from a state of low oxygen is expected if the environmental conditions are transient. If levels do drop below 4 mg/l negative effects on these organisms can be expected with adverse effects occurring below 2 mg/l (Cole et al., 1999). No information was found regarding Sabellaria spinulosa tolerance to changes in oxygenation. 

Sensitivity Assessment. Reduced oxygen levels are likely to inhibit photosynthesis and respiration but not cause a loss of the macroalgae population directly.  However, small invertebrate epifauna may be lost, causing a reduction in species richness. Therefore, a resistance of ‘High’ is recorded.  Resilience is assessed as ‘High’, and the biotope is assessed as ‘Not sensitive’ at the benchmark level.

Nutrient enrichment

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

Evidence

Holt et al. (1995) suggest that Laminaria hyperborea may be tolerant of nutrient enrichment since healthy populations are found at ends of sublittoral untreated sewage outfalls in the Isle of Man. Increased nutrient levels e.g. from sewage outfalls have been associated with increases in abundance, primary biomass and Laminaria hyperborea stipe production but with concomitant decreases in species numbers and diversity (Fletcher, 1996).  Increased nutrients may result in phytoplankton blooms that increase turbidity (see above). Increased nutrients may favour sea urchins, e.g. Echinus esculentus, due to their ability to absorb dissolved organics, and result in increased grazing pressure leading to loss of understorey epiflora/fauna, decreased kelp recruitment and possibly 'urchin barrens'. Therefore, although nutrients may not affect kelps directly, indirect effects such as turbidity, siltation and competition may significantly affect the structure of the biotope.

No direct evidence was found of the effects of nutrient enrichment on Sabellaria spinulosa crusts and reefs. However, this biotope is considered to be 'Not sensitive' at the pressure benchmark, that assumes compliance with good status as defined by the WFD.

Organic enrichment

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

Evidence

Holt et al. (1995) suggest that Laminaria hyperborea may be tolerant of organic enrichment since healthy populations are found at ends of sublittoral untreated sewage outfalls in the Isle of Man. Increased nutrient levels e.g. from sewage outfalls have been associated with increases in abundance, primary biomass and Laminaria hyperborea stipe production but with concomitant decreases in species numbers and diversity (Fletcher, 1996). Increase in ephemeral and opportunistic algae is associated with reduced numbers of perennial macrophytes (Fletcher, 1996). Increased nutrients may also result in phytoplankton blooms that increase turbidity. Therefore, although organic enrichment may not affect kelps directly, indirect effects such as turbidity may significantly affect the structure of Laminaria hyperborea biotopes.

Sabellaria spinulosa was reported to show enhanced growth adjacent to a sludge dumping area in Dublin Bay (Walker & Rees 1980).  Hence, Sabellaria spinulosa reef biotopes are probably resistant to a high level of organic enrichment.  Information on the levels of organic matter in Dublin Bay was not provided and so it is unclear how the levels experienced relate to the pressure benchmark. Sabellaria spinulosa reefs are found in areas of high water movement of up to 1 m/s (Pearce et al., 2014) that would naturally disperse some organic matter preventing accumulation and siltation.  In larger, dense colonies of Sabellaria spinulosa, sand, detritus, and finer faecal materials collect in between worm tubes.  These detritus layers do not interrupt the normal growth of the individuals or the colony as a whole (Schafer, 1972).  Hence, it seems likely that Sabellaria spinulosa crusts and reefs are resistant to the deposition of a fine layer of organic materials.

Indirect effects arising from inputs of organic matter are possible where habitat quality and species interactions are altered.  In the Wadden Sea, large subtidal areas of Sabellaria spinulosa reefs have been completely lost since the 1920s.  This decline was partly attributed to an increase in coastal eutrophication that favoured blue mussel beds (Dörjes, 1992; Hayward & Ryland, 1998; Benson et al., 2013).  However, a direct causal link has not been established and it is possible that the decline of Sabellaria spinulosa reefs was due to physical damage from fishing activities rather than competitive interactions (Jones et al., 2000).

Sensitivity assessment. Little evidence was found to support this sensitivity assessment. Sabellaria spinulosa and the associated species assemblage (which typically includes attached filter feeders from several phyla) is likely to be able to consume extra organic matter.  This conclusion is supported by the enhanced growth rates recorded in the vicinity of sewage disposal areas (Walker & Rees, 1980). However, the Laminaria canopy and especially epiphytes and red algal epiflora may experience a reduction in abundance due to increased turbidity and competition with opportunistic green algae. Therefore, resistance is assessed as 'Medium' as a precaution, albeit with 'Low' confidence. Hence, resilience is assessed as 'High' and the sensitivity of this biotope as 'Low'.

Physical loss (to land or freshwater habitat)

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

Evidence

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 rock substrata were replaced with sedimentary substrata this would represent a fundamental change in habitat type, which Laminaria hyperborea would not be able to tolerate (Birkett et al., 1998b). Sabellaria spinulosa also develops crusts and reefs on coarse sediment and could probably recover.  However, the biotope would no longer be a rock habitat, would lose its macroalgal component and be lost. Therefore, resistance to the pressure is assessed 'None' and resilience 'Very Low' so that 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

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

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

Christie et al. (1998) observed Laminaria hyperborea habitat regeneration following commercial Laminaria hyperborea trawling in south Norway. Within the study area, trawling removed all large canopy-forming adult Laminaria hyperborea. However, sub-canopy recruits were largely unaffected. In 2-6 years of harvesting, a new canopy had formed one metre off the seabed. The associated holdfast communities recovered in six years, however, the epiphytic stipe community did not fully recover within the same period. Christie et al. (1998) suggested that kelp habitats were relatively resistant to direct disturbance/removal of Laminaria hyperborea canopy.  Recurrent disturbance occurring at a smaller time scale than the recovery period of 2-6 years (stated above) could extend recovery time. Kain (1975) cleared sublittoral blocks of Laminaria hyperborea at different times of the year for several years. The first colonizers and succession community differed between blocks and the time of year the blocks were cleared. However, the blocks were dominated by Laminaria hyperborea within two years of clearance. Leinaas & Christie (1996) also observed Laminaria hyperborea re-colonization of 'urchin barrens', following the removal of urchins. The substratum was initially colonized by filamentous macroalgae and Saccharina latissima but Laminaria hyperborea dominated the community after 2-4 years.

Sabellaria spinulosa reef biotopes are directly exposed to physical damage that affects the surface. Gibb et al. (2014) found no direct evidence for impacts of the surface only for Sabellaria spinulosa.  Studies of intertidal reefs of the congener Sabellaria alveolata (Cunningham et al., 1984)  found that the reef recovered within 23 days from the effects of trampling (i.e. treading, walking or stamping on the reef structures) by repairing minor damage to the worm tube porches.  Severe damage caused by kicking and jumping on the reef structure, resulted in large cracks between the tubes, and removal of sections (ca 15 x15 x10 cm) of the structure (Cunningham et al., 1984).  Subsequent wave action enlarged the holes or cracks.  However, after 23 days, at one site, one side of the hole had begun to repair, and tubes had begun to extend into the eroded area. 

Vorberg (2000) used video cameras to study the effect of shrimp fisheries on Sabellaria alveolata reefs in the Wadden Sea.  The imagery showed that a 3 m beam trawl easily ran over a reef that rose to 30 to 40 cm, although the beam was occasionally caught and misshaped on the higher sections of the reef.  At low tide, there were no signs of the reef being destroyed and, although the trawl had left impressions, all traces had disappeared four to five days later due to the rapid rebuilding of tubes by the worms.  The daily growth rate of the worms during the restoration phase was significantly higher than undisturbed growth, that is, the growth rate of undisturbed tubes was 0.7 mm/day but after removal of 2 cm of surface it was 4.4 mm/day), which indicated that as long as the reef is not completely destroyed recovery can occur rapidly. 

Sabellaria spinulosa reefs are thought to be more fragile than Sabellaria alveolata (B. Pearce, pers. comm., cited from Gibb et al., 2014) and, therefore, surface abrasion may lead to greater damage and lower recovery rates than observed for Sabellaria alveolata.  Sabellaria spinulosa reefs are often only approximately 10 cm thick, surface abrasion can, therefore, severely damage and/or remove a reef. No direct observations of reef recovery, through repair, from abrasion were found for Sabellaria spinulosa.

Sensitivity assessment. Based on the evidence discussed above, abrasion at the surface of Sabellaria spinulosa crusts is likely to damage the tubes and result in sub-lethal and lethal damage to the worms. It is also likely to remove a proportion of the Laminaria canopy, attached epiphytes, Laminaria holdfasts and understorey macroalgae (where present). Therefore, resistance is assessed as ‘Low’ (loss of 25-75% of the extent/abundance of component species within the impact footprint).  Hence, resilience is assessed as ‘Medium’ (within 2-10 years) and sensitivity 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

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

Suspended Particle Matter (SPM) concentration has a linear relationship with subsurface light attenuation (Kd) (Devlin et al., 2008).  An increase in SPM results in a decrease in sub-surface light attenuation.  Light availability and water turbidity are principal factors that determine the depth range of Laminaria hyperborea (0-47 m Below Sea Level) (Birkett et al., 1998b).  Light penetration influences the maximum depth at which kelp species can grow and it has been reported that laminarians grow at depths at which the light levels are reduced to one per cent of incident light at the surface.  Maximal depth distribution of laminarians, therefore, varies from 100 m in the Mediterranean to only 6-7 m in the silt-laden German Bight.  In Atlantic European waters, the depth limit is typically 35 m.  In very turbid waters, the depth at which Laminaria hyperborea is found may be reduced to 2.5 m (Birkett et al. 1998b), or in some cases excluded completely (e.g. Severn Estuary), because of the alteration in light attenuation by suspended sediment (Birkett et al. 1998b; Lüning, 1990).

Laminaria spp. show a decrease of 50% photosynthetic activity when turbidity increases by 0.1 /m (light attenuation coefficient =0.1-0.2 /m; Staehr & Wernberg, 2009).  An increase in water turbidity will likely affect the photosynthetic ability of Laminaria hyperborea and decrease its abundance and density (see IR.HIR.KFaR.LhypR.Pk).  Kain (1964) suggested that early Laminaria hyperborea gametophyte development could occur in the absence of light.  Furthermore, observations from south Norway found that a pool of Laminaria hyperborea recruits could persist growing beneath Laminaria hyperborea canopies for several years, indicating that sporophytes growth can occur in light-limited environments (Christie et al., 1998).  However, in habitats exposed to high levels of suspended silts, Laminaria hyperborea is out-competed by Saccharina latissima, a silt tolerant species. Thus, a decrease in water clarity is likely to decrease the abundance of Laminaria hyperborea in the affected area (Norton, 1978).  The biotope is expected to be excluded from silt rich environments.

Sabellaria spinulosa do not rely on light penetration for photosynthesis, it is also believed that visual perception is limited and that this species does not rely on sight to locate food or other resources.  In a recent review of the sensitivity of Sabellaira spinulosa reefs to anthropogenic disturbance, Fariñas-Franco et al. (2014) concluded that impacts on Sabellaria spinulosa due to a decrease in water clarity resulting from an increase in suspended solids (inorganic or organic) are unlikely, although no thresholds regarding tolerance or intolerance were found.  Decreases in suspended particles that reduce the supply of food or tube-building materials may, however, negatively impact this species (Davies et al., 2009; Last et al., 2011).

Sabellaria spinulosa relies on a supply of suspended solids and organic matter to filter feed and build protective tubes and so they are often found in areas with high levels of turbidity.  Davies et al. (2009) and Last et al. (2011) developed Vortex Resuspension Tanks (VoRT)  to test the effects of a change in the composition of suspended sediment on benthic species.  This laboratory experiment manipulated turbidity and current flow and demonstrated the susceptibility of Sabellaria spinulosa to a decrease in suspended particulate matter (SPM).  A clear erosion of tubes was observed in the absence of SPM and subsequent starvation of tube building materials.  At high and intermediate sediment regimes (high SPM ~71 mg/l) conditions were comparable to what might be expected within only a few hundred meters distance of a primary aggregate extraction site and Sabellaria spinulosa maintained a cumulative growth rate at these rates of SPM.  This supports the view that the availability of suspended particles is necessary for Sabellaria spinulosa development and that tolerance of elevated levels is likely (Davies et al., 2009). Indirect evidence for the tolerance of Sabellaria spinulosa for changes in turbidity is provided by the persistence of reefs on the outskirts of aggregate dredging areas (Pearce et al., 2007, 2011a), which appear unaffected by dredging that is likely to have led to sediment plumes.  Such plumes, however, are short-lived (Tillin et al., 2011) and, therefore, the long-term effect depends on the duration of dredging activities.

Tillin (2010) used logistic regression to develop statistical models that indicate how the probability of occurrence of the congener Sabellaria alveolata changes over environmental gradients within the Severn Estuary. The modelled ranges should be interpreted with caution and apply to the Severn Estuary alone (which experiences large tidal ranges, high currents and extremely high suspended sediment loads and is therefore distinct from many other estuarine systems).  The models indicate that the optimal mean neap sediment concentrations for subtidal Sabellaria alveolata range from 515.7 to 906 mg/l and optimal mean spring sediment concentrations range from 855.3 to 1631 mg/l.  Although not directly applicable to Sabellaria spinulosa this data suggests that tube-building sabellariids are tolerant to very high levels of suspended sediment.  Fine sediments such as mud may clog the gills and feeding tentacles of some polychaetes and, therefore, the potential impact will be mediated by the character of the sediment in suspension.

Sensitivity assessment. The benchmark for this pressure refers to a change in turbidity of one rank, e.g. from clear (<10 mg/l) to intermediate (10-100 mg/l) or intermediate to medium (100-300 mg/l).  Sabellaria spinulosa do not photosynthesise and do not rely on sight to locate resources and therefore no effects are predicted for reef biotopes from an increase or decrease in clarity resulting from a change in one rank on the water framework directive scale.  Experiments (Davies et al., 2009) and predictive modelling (Tillin, 2010) indicate that tube building sabellariids can tolerate a broad range of suspended solids so the Sabellaria crusts are unlikely to be affected by an increase in suspended sediment. However, if the supply of sand to the habitat was reduced, then the Sabellaria crusts would probably erode and be replaced with a diverse understorey of red algae, similar to IR.MIR.KR.Lhyp.  Similarly, an increase in turbidity will reduce the abundance of the Laminaria hyperborea canopy, especially in deeper examples of the biotope, and the Laminaria may be replaced by Saccharina latissima or by an abundant Sabellaria crust similar to CR.MCR.CSab.Sspi. Overall, the biotope is likely to change in character, be reclassified, and, effectively, lost. Therefore, resistance is assessed as ‘Low’,  resilience as ‘Medium’, and sensitivity is assessed as 'Medium'.

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

Smothering by sediment (e.g. 5 cm of fine material) in a discrete event is unlikely to damage Laminaria hyperborea sporophytes but is likely to affect gametophyte survival as well as holdfast fauna, and interfere with zoospore settlement.  Given the microscopic size of the gametophyte, 5 cm of sediment could be expected to significantly inhibit growth. However, laboratory studies showed that gametophytes can survive in darkness for between 6 and 16 months at 8°C and would probably survive smothering by a discrete event.  Once returned to normal conditions the gametophytes resumed growth or maturation within one month (Dieck, 1993). Intolerance to this factor is likely to be higher during the peak periods of sporulation and/or spore settlement. If inundation is long-lasting then the understorey epifauna/flora may be adversely affected, e.g. suspension or filter-feeding fauna and/or algal species.  However, this biotope is found in sand-laden waters (JNCC, 2015) so that the understorey of red algae and epifauna is limited in abundance.

Sabellaria spinulosa is often found in areas of high water movement with some degree of sediment transport essential for tube-building and feeding.  Sabellaria spinulosa reefs adjacent to aggregate dredging areas appear unimpacted by dredging operations (Pearce et al., 2007; Pearce et al., 2011a).  Evidence suggests that given the dynamic sedimentary environments in which sabellariids live, their populations can certainly persevere in turbid conditions despite ‘typical’ natural levels of burial (Last et al., 2011) and that recovery from burial events is high. Last et al. (2011) buried Sabellaria spinulosa worms (isolated into artificial tubes), under three different depths of sediment – shallow (2 cm), medium (5 cm) and deep (7 cm).  The results indicated that Sabellaria spinulosa could survive short-term (32 days), periodic, burial by sand of up to 7 cm.  Last et al. (2011) suggested that the formation of ‘emergence tubes’ (newly created tubes extending to the surface) under sediment burial allowed Sabellaria spinulosa to tolerate gradual burial and that perhaps this mechanism allows for continued adult dispersal.  This mechanism occurred most rapidly throughout the 8-day burial at ~1 mm per day (Last et al., 2011).  But even though tube-growth still seems possible under burial, the dumping of fine and coarse material will probably block feeding apparatus and, therefore, worm development will be curtailed.

Sensitivity assessment. This biotope occurs in moderately wave exposed conditions so that deposited sediments are unlikely to remain for more than a few tidal cycles and the effects of a deposit of 5 cm of fine sediment in a discrete event are likely to be transient. In addition, both Laminaria hyperborea and Sabellaria spinulosa crusts are unlikely to be adversely affected by a light deposition of 5 cm of sediment.   Therefore, resistance to the pressure is assessed as ‘High’, and resilience as ‘High’ so that sensitivity is assessed as ‘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

Smothering by sediment (e.g. 30 cm of fine material) in a discrete event is unlikely to damage Laminaria hyperborea plants but is likely to affect gametophyte survival, holdfast communities, the epiphytic community at the base of the stipe, and interfere with zoospore settlement. Given the microscopic size of the gametophyte, 30 cm of sediment could be expected to significantly inhibit growth. However, laboratory studies showed that gametophytes can survive in darkness for between 6 and 16 months at 8°C and would probably survive smothering within a discrete event. Once returned to normal conditions the gametophytes resumed growth or maturation within 1 month (Dieck, 1993). Intolerance to this factor is likely to be higher during the peak periods of sporulation and/or spore settlement.  If clearance of deposited sediment occurs rapidly then understorey communities are expected to recover quickly. If inundation is long-lasting then the understorey epifauna/flora may be adversely affected, e.g. suspension or filter-feeding fauna and/or algal species.  However, this biotope is found in sand-laden waters (JNCC, 2015) so that the understorey of red algae and epifauna is limited in abundance.

Sabellaria spinulosa is often found in areas of high water movement with some degree of sediment transport essential for tube-building and feeding. Sabellaria spinulosa reefs adjacent to aggregate dredging areas appear unimpacted by dredging operations (Pearce et al., 2007; Pearce et al., 2011a).  Evidence suggests that the dynamic sedimentary environments in which sabellariids live, their populations can persevere in turbid conditions in spite of ‘typical’ natural levels of burial (Last et al., 2011) and that recovery from burial events is high.  The congener Sabellaria alveolata was reported to survive short-term burial for days and even weeks in the south-west as a result of storms that altered sand levels up to two meters, although they were, killed by longer-term burial (Earll & Erwin 1983).

Last et al. (2011) buried Sabellaria spinulosa worms (isolated into artificial tubes), under three different depths of sediment – shallow (2 cm), medium (5 cm) and deep (7 cm).  The results indicate that Sabellaria spinulosa can survive short-term (32 days), periodic burial by sand of up to 7 cm.  Last et al. (2011) suggested that the formation of ‘emergence tubes’ (newly created tubes extending to the surface) under sediment burial allowed Sabellaria spinulosa to tolerate gradual burial and that perhaps this mechanism allows for continued adult dispersal.  This mechanism occurred most rapidly throughout the 8-day burial at ~1 mm per day (Last et al., 2011) but even though tube-growth still seems possible under burial, it is likely that the dumping of fine and coarse material will block feeding apparatus and, therefore, worm development will be curtailed. 

A Sabellaria spinulosa reef off the coast of Dorset showed periodic burial from large sand waves (Collins, 2003).  The displacement of some colonies that had established themselves on a gas pipeline 1 km off the coast of Aberdeen was also associated with burial (Mistakidis, 1956; cited by Holt et al., 1998).  Furthermore the loss of a 2 km² area of Ross worm reef in Jade Bay, North Sea was attributed to burial as a consequence of mud deposition, although fishing activity may have contributed to the decline (Dörjes, 1992, cited from Hendrick et al., 2011). The evidence above suggests that Sabellaria spinulosa reefs are sensitive to damage from siltation events (Hendrick et al., 2011).  However, recovery is likely to be rapid given that larval dispersal is not interrupted and new reefs are likely to be able to establish themselves over old buried ones as postulated by (Fariñas-Franco et al., 2014).

Sensitivity assessment. No direct evidence was found for the length of time that Sabellaria spinulosa can survive beneath 30 cm of sediment.  Although this biotope occurs in moderate energy habitats (due to wave action), deposition of 30 cm of sediment represents a large volume of material that would probably remain for a number of tidal cycles and is expected to damage understorey flora/fauna as well as juvenile Laminaria hyperborea.   Similarly, burial to Sabellaria crusts to a depth 30 cm of fine sediment may also result in loss the abundance or extent of the crusts, based on the observations in Hendrick et al. (2011).  Therefore, as a precautionary assessment, resistance is assessed as ‘Low’ due to the depth of overburden. Hence, resilience is assessed as ‘Medium’ (2-10 years) and sensitivity as ‘Medium’.  

Litter

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

Evidence

Electromagnetic changes

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

Evidence

Underwater noise changes

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

Evidence

Introduction of light or shading

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

Evidence

Shading of the biotope (e.g. by construction of a pontoon, pier etc) could adversely affect the biotope in areas where the water clarity is also low, and tip the balance to shade tolerant species, resulting in the loss of the biotope directly within the shaded area, or a reduction in laminarian abundance from forest to park type biotopes.

Sensitivity assessment. Resistance is probably 'Low', with a 'Medium' resilience and a sensitivity of 'Medium', albeit with 'low' confidence due to the lack of direct evidence.

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

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

Visual disturbance

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

Evidence

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

None of the important structuring characteristic species (e.g. Laminaria hyperborea or Sabellaria spinulosa) are subject to genetic modification or translocation, at present. Therefore, this pressure is considered 'Not relevant'. 

Introduction or spread of invasive non-indigenous species

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

Evidence

Competition with invasive macroalgae may be a potential threat to this biotope. Potential invasives include Undaria pinnatifida, Sargassum muticum and Codium fragile. Sargassum muticum has been shown to competitively replace Laminaria spp. in Denmark (Staehr et al., 2000). In Nova Scotia, Codium fragile competes successfully with native kelps for space including Laminaria digitata, exploiting gaps within the kelp beds. Once established the algal mat created by Codium fragile prevents re-colonization by other macro-algae (Scheibling et al., 2006).

Sargassum muticum is a circumglobal invasive species (Engelen et al., 2015). It is recorded (2015) from Norway to Morocco and into the Mediterranean in the eastern Atlantic, from Alaska to Baja California in the eastern Pacific, and from southern Russia to southern China in the western Pacific (Engelen et al., 2015). It colonizes a variety of habitats and can tolerate -1°C to 30°C and survive salinities below 10 ppt.  Although fertilization does not occur below 15 ppt and growth of germlings is limited below 10°C, it can complete its life cycle as long as temperatures are over 8°C for at least four months of the year (Engelen et al., 2015).  However, its distribution is limited by the availability of hard substratum (e.g., stones >10 cm) and light (Staeher et al., 2000; Strong & Dring 2011; Engelen et al., 2015). It is most abundant between 1 and 3 m below mean water, but it has been recorded at 18 m or 30 m in the clear waters of California. However, it is a poor competitor under low light and only develops dense canopies in shallow areas (Engelen et al., 2015).

Sargassum muticum was shown to replace and out-compete leathery, canopy-forming macroalgae such as Saccharina latissima, Halidrys siliquosa, and Fucus spp. and, to a lesser degree, understorey species such as Codium fragile, Chondrus crispus and Dictyota dichotoma in Limfjorden, Denmark between 1984 and 1997 (Staehr et al., 2000; Engelen et al., 2015; de Bettignies et al., 2021). The invasion in Limfjorden had stabilized by 2005 although many of the native macroalgal species continued to decline (Engelen et al., 2015). In Limfjorden, the distribution of Sargassum muticum was limited to areas with hard substratum, in particular stones >10 cm in diameter, while smaller stones, gravel and sand were unsuitable. It was most abundant between 1 and 4 m in depth but had low cover at 0 to 0.5 m or 4 to 6 m, in the turbid waters of the Limfjorden. Limfjorden is wave sheltered although wave exposure has been reported to restrict the growth and survival of Sargassum muticum (Staehr et al., 2000). Viejo et al. (1995) reported that Sargassum muticum transplanted to wave exposed shores in Spain experienced >80% breakages within a month and that the growth of undamaged plants was significantly lower than that of plants on sheltered shores.  Similarly, Andrew & Viejo (1998) noted that Sargassum muticum was restricted to intertidal rockpools in wave exposed sites in the Bay of Biscay.

Strong & Dring (2011) used canopy removal experiments to investigate inter- and intra-species competition between Sargassum muticum and Saccharina latissima in the Dorn, Strangford Lough, N. Ireland. The Dorn consists of tidal pools, very sheltered from wave action but with moderately strong tidal streams (1-2 knots). Sargassum muticum grew better in mixed stands with Saccharina latissima than in the highest density monospecific stands examined. However, the growth of Saccharina was not affected by the proportion of Sargassum in mixed stands. They concluded that Saccharina was not impacted significantly by the alien species while Sargassum benefited from growth in mixed stands. Experimental manipulation of subtidal algal canopies in the San Juan Islands, Washington State, USA, showed that Sargassum muticum reduced the abundance of native macroalgae, including the kelp Laminaria bongardiana due to shading. However, the experimental removal of Sargassum resulted in the recovery of native species within about 1 year (Britton-Simmons, 2004; Engelen et al., 2015). The negative effects of Sargassum muticum on native macroalgae are mainly due to competition for light, rather than changes in nutrient availability, sedimentation, or water flow (Britton-Simmons, 2004; Engelen et al., 2015). Cosson (1999) reported a significant decline in Laminaria digitata at two sites between 1983 and 1997 on the coast of Normandy, France, due to an increase in Sargassum muticum abundance in the same areas. For example, on the Grandcamp rocks, Laminaria digitata has almost disappeared while Sargassum muticum had covered 80% of the lower intertidal and subtidal zone in summer.

Undaria pinnatifida (Wakame or Asian kelp) is a large brown seaweed and an Invasive Non-Indigenous Species (INIS) that could out-compete native UK kelp species (see Farrell & Fletcher, 2006; Thompson & Schiel, 2012; Brodie et al., 2014; Hieser et al., 2014; Arnold et al., 2016; Epstein & Smale, 2017; Epstein & Smale, 2018; Kraan, 2017; Epstein et al., 2019a,b; Tidbury, 2020). Undaria pinnatifida originates from Japan but is established currently on the coastlines of New Zealand, Australia, Northern France, Spain, Italy, the UK, Portugal, Belgium, Holland, Argentina, Mexico, and the USA (De Leij et al., 2017). Undaria pinnatifida was first recorded in the UK in the Hamble Estuary in 1994 (Macleod et al., 2016). It has since proliferated along UK coastlines. One year after its discovery at the Queen Anne Battery marina, Plymouth, it became a major fouling plant on pontoons (Minchin & Nunn, 2014). Although initially restricted to artificial habitats, such as marinas and ports, it is now widespread in natural habitats in several areas, including Plymouth Sound.

Undaria pinnatifida seems to settle better on artificial substrata (e.g., floats, marinas, or piers) than on natural rocky shores among local kelps (Vaz-Pinto et al., 2014). It is found predominantly in low intertidal to shallow subtidal habitats (Epstein et al., 2019b) and is significantly more abundant on artificial substrata compared to natural rocky substrata (Heiser et al., 2014; Epstein & Smale, 2018).  James (2017) suggested that Undaria pinnatifida could out-compete native species on artificial substrata (such as marinas and wharf structures). In Plymouth, UK, De Leij et al. (2017) found that natural habitats with dense native macroalgal canopies, such as Laminaria hyperborea, Laminaria ochroleuca, Laminaria digitata and Saccharina latissima had more resistance to Undaria pinnatifida invasion than disturbed or sparse canopies, due to limited space and light availability for Undaria pinnatifida recruits. However, the dense canopies did not always prevent invasion of Undaria pinnatifida as sporophytes were still recorded within dense Laminaria canopies, so that canopy disturbance was not always required (De Leij et al., 2017; Epstein & Smale, 2018).

Undaria pinnatifida species behaves as a winter annual and recruitment occurs in winter followed by rapid growth through spring, maturity and then senescence through summer, with only the microscopic life stages persisting through autumn. It exhibits multiple dispersal strategies, such as short-range spore dispersal, and long-range dispersal as whole drift plants or fragments. Undaria pinnatifida has spread rapidly across the UK and Europe, resulting in community-wide responses and impacts (Vaz-Pinto et al., 2014; Epstein & Smale, 2017). Its impacts are complex and context-specific, depending on space, time, and taxa present in the introduced location (Epstein & Smale, 2017; Teagle et al., 2017; Tidbury, 2020).

Undaria pinnatifida has a wide physiological niche meaning it can occur in both coastal and estuarine environments showing tolerance for varying salinities, turbidity, and siltation (Heiser et al., 2014; Epstein & Smale, 2018). Undaria pinnatifida prefers sheltered sites with low wave exposure and weak tidal streams (Heiser et al., 2014; Epstein & Smale, 2018). In natural habitats, Undaria pinnatifida was not recorded if the wave fetch was greater than 642 km but increased in abundance and cover in very sheltered sites (Epstein & Smale, 2018).

In St Malo, France, there was evidence that Undaria pinnatifida could co-exist with Laminaria digitata under certain conditions (Castric-Fey et al., 1993). Epstein et al. (2019b) observed that, in Plymouth Sound, UK, Undaria pinnatifida co-existed with seven species of canopy-forming brown macroalgae within its depth range (+1 to –4 m), including Laminaria digitata; which suggested that they could occupy an overlapping niche. Epstein & Smale (2018) also observed that Undaria pinnatifida was relatively common (abundance of >70 individuals per 25 m transect) at three sites in Devon, UK (Jennycliff, Bovisand and Beacon Cove) where Laminaria spp. were abundant (40-79%) or superabundant (>80%), which suggested that Undaria pinnatifida could co-exist within refugia amongst areas with dense Laminaria spp..

In many cases, Undaria pinnatifida seems to have minimal impacts on native communities (e.g., Forrest & Taylor, 2002; Valentine & Johnson, 2003; South et al., 2016; Epstein & Smale, 2017; Epstein & Smale 2018). Laminaria digitata forms dense monospecific canopies and its thick, extensive laminae are likely to restrict light penetration to the underlying substratum, including Undaria pinnatifida (De Leij et al., 2017). Disturbance to the native kelp canopy can facilitate the spread of INIS by increasing the availability of resources such as light and space. Experimental full removal of the existing kelp canopy in Plymouth Sound allowed the mean cover of Undaria pinnatifida to increase from ca 10% to ca 50% within three months (De Leij et al., 2017). Their experiment showed that the density of Laminaria digitata was important to Undaria pinnatifida invasion (De Leij et al., 2017).

Similarly, a primary succession experiment by Epstein et al. (2019b) in Plymouth Sound (UK) showed that clearance of Laminaria digitata in 2016 increased Undaria pinnatifida abundance. However, this was quickly followed by the recovery of Laminaria digitata in 2017 and the concurrent decline in Undaria pinnatifida, which suggested that Laminaria digitata had a higher fitness (Epstein et al., 2019b). Within the same study, Epstein et al. (2019b) observed that Undaria pinnatifida exhibited a significant negative relationship with Laminaria digitata on intertidal rocky reef substrata, which suggested that Laminaria digitata negatively affected Undaria pinnatifida abundance. It was also suggested that Undaria pinnatifida has a lower resistance to desiccation than Laminaria digitata. As a result, Epstein & Smale (2019b) concluded that due to its lower fitness, Undaria found within natural habitats in the northeast Atlantic has low ecological and community level impacts and was competitively inferior to Laminaria spp.. However, Heiser et al. (2014) found that in Plymouth, UK, Laminaria digitata was significantly less abundant at sites with the presence of Undaria pinnatifida, with only ca 1.5 Laminaria digitata individuals per m² with Undaria pinnatifida, compared to ca 7 individuals per m² at sites without Undaria pinnatifida. Undaria pinnatifida was successfully eradicated on a sunken ship in Chatham Islands, New Zealand, by applying a heat treatment of 70°C (Wotton et al., 2004). However, numerous other eradication attempts have failed and as noted by Fletcher & Farrell (1998), once established Undaria pinnatifida resists most attempts at long-term removal.

Moreover, the Pacific oyster Magallana gigas potentially pose a threat to Sabellaria spinulosa reefs or crusts. Reefs of Sabellaria alveolata in the bay of Le Mont-Saint-Michel, France are becoming increasingly colonized by the pacific oyster Magallana gigas (Dubois et al. 2006). Given the high filtration rates of Magallana gigas, it is believed that they can out-compete Sabellaria alveolata for feeding resources (Dubois et al., 2006). In the Wadden Sea, Magallana gigas have replaced blue mussels (Foster-Smith, 2000) suggesting that Magallana gigas may impact filter-feeding, reef-forming organisms in general. The reasons underlying the species shift from Mytilus edulis to Magallana gigas have not been elucidated, however, and may be due to recent changes in climatic conditions (Thieltges, 2005) rather than competitive interactions. It should be noted that even though Magallana gigas is distributed throughout UK waters following an initial introduction in 1926 (Linke, 1951) there is currently no evidence, in the absence of any targeted studies, that this species is impacting native Sabellaria spinulosa or Sabellaria alveolata reefs (Hendrick, et al. 2011). 

Sensitivity assessment. The above evidence suggests that Undaria pinnatifida can co-exist with Laminaria hyperborea where sites are suitable e.g., Laminaria hyperborea in Plymouth Sound, UK. A dense kelp canopy may restrict or slow the proliferation of Undaria pinnatifida, however, there is mixed evidence of its colonization with Laminaria hyperborea beds and in some areas, a lower abundance of Laminaria hyperborea may result in increased Undaria pinnatifida growth. Moreover, Magallana gigas may pose a potential threat in terms of competition for food and space so this assessment may require updating in the future as the distributions and interactions between these species are better understood.  

This biotope (IR.MIR.KR.Lhyp.Sab) is found within the infralittoral zone with moderate exposure to wave action and weak tidal streams. The evidence above suggests that Sargassum muticum prefers wave sheltered, shallow sites in the sublittoral fringe. It was reported to out-compete and replace Saccharina latissima in the Limfjorden and achieve maximum abundance between 1 and 4 m (Staehr et al., 2000; Engelen et al., 2015) but no evidence of the effects of Sargassum on Laminaria hyperborea beds was found. However, Sargassum is unlikely to survive in this biotope due to the wave exposed conditions within this biotope and due to the scouring it will be unable to gain a foothold.

Undaria has the potential to colonize and co-exist in refugia within Laminaria sp. dominated habitats, especially in shallow examples of their biotopes, sheltered from wave action. However, like Sargassum, even in the shallow sites Undaria is unlikely to survive either the sand scouring, as it will be unable to gain a foothold, or the high degree of wave exposure that characterizes this biotope. Therefore, resistance to Sargassum or Undaria is assessed as ‘High’, resilience as 'High', and sensitivity is assessed as ‘Not Sensitive’. Overall, confidence is assessed as ‘Low’ due to evidence of variation and the site-specific nature of competition between native kelps and Undaria pinnatifida.   

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

Galls on the blade of Laminaria hyperborea and spot disease are associated with the endophyte Streblonema sp. although the causal agent is unknown (bacteria, virus or endophyte). The resultant damage to the blade and stipe may increase losses in storms. The endophyte inhibits spore production and, therefore, recruitment and recoverability (Lein et al., 1991). However, no evidence was found for adverse impacts of microbial pathogens on Sabellaria spinulosa.   Therefore, resistance to the pressure is assessed as ‘Medium’, based on the possible effects on Laminaria hyperborea. However, resilience is probably ‘High’ so that 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

Christie et al. (1998) observed Laminaria hyperborea habitat regeneration following commercial Laminaria hyperborea trawling in south Norway. Within the study area trawling removed all large canopy-forming adult Laminaria hyperborea, however, sub-canopy recruits were unaffected. Within 2-3 years of harvesting, a new canopy had formed one metre off the seabed. The associated holdfast communities recovered in six years, however, the epiphytic stipe community did not fully recover within the same period. Christie et al. (1998) suggested that kelp habitats were relatively resistant to direct disturbance of Laminaria hyperborea canopy.

Recurrent disturbance occurring at a smaller time scale than the recovery period of 2-6 years (stated above) could extend recovery time. Kain (1975) cleared sublittoral blocks of Laminaria hyperborea at different times of the year for several years. The first colonizers and succession community differed between blocks and the time of year the blocks were cleared.  However, within 2 years of clearance, the blocks were dominated by Laminaria hyperborea. Leinaas & Christie (1996) observed Laminaria hyperborea re-colonization of “urchin barrens”, following removal of urchins. The substratum was initially colonized by filamentous macroalgae and Saccharina latissima but Laminaria hyperborea dominated the community after 2-4 years. Following disturbance or in areas were recurrent rapid disturbance occurs Laminaria hyperborea recruitment could also be affected by interspecific competitive interactions with Invasive Non-Indigenous Species or ephemeral algal species (Brodie et al., 2014; Smale et al., 2013), however, evidence for this is limited and thus not included within this assessment. Sabellaria spinulosa has no economic value and is not commercially harvested and itself is not directly impacted by this pressure. 

Sensitivity assessment. Therefore, resistance is assessed as ‘None’, and resilience ‘Medium’ so that the sensitivity of this biotope to the removal of target species is assessed as ‘Medium’.

Removal of non-target species

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

Evidence

Incidental/accidental removal of Laminaria hyperborea from extraction of other marine resources, e.g. fisheries or aggregates, is likely to cause similar effects to that of direct harvesting of Laminaria hyperborea.  Hence, the same evidence has been used for both pressure assessments. Christie et al. (1998) observed Laminaria hyperborea habitat regeneration following commercial Laminaria hyperborea trawling in south Norway. Within the study area trawling removed all large canopy-forming adult Laminaria hyperborea, however, sub-canopy recruits were unaffected. Within 2-3 years of harvesting, a new canopy had formed one metre off the seabed. The associated holdfast communities recovered in six years, however, the epiphytic stipe community did not fully recover within the same period. Christie et al. (1998) suggested that kelp habitats were relatively resistant to direct disturbance of Laminaria hyperborea canopy.

Recurrent disturbance occurring at a smaller time scale than the recovery period of 2-6 years (stated above) could extend recovery time. Kain (1975) cleared sublittoral blocks of Laminaria hyperborea at different times of the year for several years. The first colonizers and succession community differed between blocks and the time of year the blocks were cleared.  However, the blocks were dominated by Laminaria hyperborea within two years of clearance. Leinaas & Christie (1996) observed Laminaria hyperborea re-colonization of 'urchin barrens', following the removal of urchins. The substratum was initially colonized by filamentous macroalgae and Saccharina latissima but Laminaria hyperborea dominated the community after 2-4 years. Following disturbance or in areas were recurrent rapid disturbance occurs Laminaria hyperborea recruitment could also be affected by interspecific competitive interactions with Invasive Non-Indigenous Species or ephemeral algal species (Brodie et al., 2014; Smale et al., 2013), however, evidence for this is limited and thus not included within this assessment. 

Sabellaria spinulosa biotopes may be removed or damaged by static or mobile gears that target other species. These direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures. Evidence for ecological interactions between Sabellaria spinulosa and other species is limited. The removal of Sabellaria spinulosa predators as by-catch may be beneficial. Sabellaria spinulosa reefs appear to be important nursery areas for commercially targeted flatfish including Dover sole (Bryony Pearce, pers comm). Assessment of this indirect effect is limited by the lack of empirical evidence for predator-prey relationships. Stomach analysis of fish by Pearce (2001) found that juvenile flatfish captured in reef areas including Dover sole, dab and plaice fed preferentially on Sabellaria spinulosa. Pearce et al. (2011b) found that butterfish Pholis gunnellus and dragonet Callionymus lyra also prey on Sabellaria spinulosa. Previous studies have also shown that Carcinus maenas feeds on Sabellaria spinulosa (Taylor, 1962; Bamber & Irving, 1997). Other invertebrates such as Pandalus montagui and Asterias rubens found in association with Sabellaria spinulosa reefs may also be feeding on the worms or other species associated with the reefs rather than Sabellaria spinulosa. Due to the limited information available on predator-prey relationships, the impact of predator removal on Sabellaria spinulosa reef biotopes cannot be assessed.  Dense aggregations of the brittle star, Ophiothrix fragilis, have been suggested to compete with Sabellaria spinulosa for space and food and potentially to consume the gametes inhibiting recruitment (George & Warwick 1985). Removal of this species as by-catch could potentially be beneficial to the reef biotopes.

Sensitivity assessment. Although the removal of predatory species by commercial fisheries may be beneficial to Sabellaria spinulosa, the accidental removal (e.g. as by-catch) of a proportion of the kelp bed and possibly the Sabellaria spinulosa crusts could impact the biotope. Therefore, resistance is assessed as 'Low' and resilience as ‘Medium’ so that sensitivity is assessed as 'Medium’.