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

Species found in the intertidal are exposed to extremes of high and low air temperatures during periods of emersion. They must also be able to cope with sharp temperature fluctuations over a short period of time during the tidal cycle. In winter, air temperatures are colder than the sea, conversely in summer air temperatures are much warmer than the sea. Species that occur in this intertidal biotope are therefore generally adapted to tolerate a range of temperatures, although the timing of site-specific factors such as low tides will influence local acclimation. For intertidal species, increased temperatures may also result in desiccation when exposed (see changes in emergence pressure). Local populations may be acclimated to the prevailing temperature regime and may, therefore, exhibit different tolerances to other populations subject to different conditions and therefore caution should be used when inferring tolerances from populations in different regions. 

Laminaria digitata is distributed from Brittany to the coast of Norway, while its UK distribution encompasses the whole of the UK coast (Blight & Thompson, 2008). Its distribution suggests that the species would tolerate chronic temperature change (e.g. by 2°C for a year). However, local populations may have acclimatized to local physical conditions meaning that populations at the extremes of the species’ range are less comparable than those populations in the middle of its range. Additionally, the distribution data of this species suggests it is a northern species, as such it will be vulnerable to increases in temperature and may be out-competed at its southern limits by other kelp species.

The thermal optimum of Laminaria digitata is between 10-15°C, with reproductive ability impaired to 20% at 18°C (Arzel, 1998). Therefore, while the current population may not be affected, recruitment may be reduced.  Spore production only occurs between 5-10°C and is the most temperature sensitive stage of reproduction in Laminaria digitata. Outside this temperature range, reproduction is severely reduced and the species is at risk from local extinction in the long-term. In addition, a temperature increase to 22-23°C causes cell damage and death (Sundene, 1964; Bolton & Lüning, 1982). The sensitivity of this species, therefore, relies on the current sea temperatures of the specific location (Bartsch et al., 2013). A minimum of 10 weeks a year between 5-18°C is needed in order to ensure spore formation and hence reproduction (Bartsch et al., 2013).

Combining predicted sea surface temperate over the next century with the current distribution of Laminaria digitata, Merzouk & Johnson (2011) predict an expansion of its northern limits and localised extinctions across its southern range edge (Mid Bay of Biscay, Northern France and southern England; Birkett et al., 1998b). Suggesting at sites where sea temperature is artificially increased as a result of anthropogenic activity (e.g. effluent output) local extinction of the biotope may occur (Raybaud et al., 2013), especially if combined with high UK summer sea temperatures in southern examples of this biotope (Bartsch et al., 2013). In southern examples of IR.MIR.KT.LdigT, Laminaria digitata may also be out-competed by its Lusitanian competitor Laminaria ochroleuca which is regionally abundant across the south UK coastline (Smale et al., 2014).

Littler & Kauker (1984) suggested that the crustose bases of Corallina officinalis are more resistant of desiccation or heating than fronds. Lüning (1990) reported that Corallina officinalis from Helgoland survived one week exposure to temperatures between 0°C and 28°C. Latham (2008) investigated the effects of temperature stress on Corallina officinalis through laboratory tests on samples collected in the autumn in Devon, (England) from rockpools. Samples were kept at 15°C for three days and then exposed to temperatures of 5°C, 15°C, 20°C, 25°C and 30°C (the normal range of temperature experienced was suggested to be between 5 and 15°C). At 35°C the Corallina was completely bleached after 3 days with a sample kept at 30°C beginning to bleach. After 7 days (the end of the experiment) the sample kept at 30°C was partially bleached. Samples kept at 5, 15, 20 and 25°C showed little change in chemicals produced in reaction to thermal stress and no bleaching suggesting the temperatures in that range had not induced stress reactions. Fronds of Osmundea pinnatifida bleach and die-back in summer, while the crustose holdfasts remain, suggesting that, as for Corallina officinalis, the bases are more resistant.  The factors responsible for the die-back are a combination of temperature (Flores-Maya et al., 1992, abstract only) desiccation and irradiance (Prathep, 2001). 

In an exceptionally hot summer (1983, with an increase of between 4.8 and 8.5°C), Hawkins & Hartnoll (1985) observed no temperature bleaching of adult Himanthalia elongata (although some buttons were bleached) or other canopy forming species. However, understorey red algae showed more signs of damage with bleached Corallina officinalis observed around the edges of pools due to desiccation. Occasional damaged specimens of Palmaria palmata, Osmundea pinnatifida and Mastocarpus stellatus were observed. Palmaria palmata does well in low temperatures, with an optimum between 6 and 15°C, consistent with a distribution in northern temperate and arctic waters. This species is also found in warmer temperate waters as far south as Portugal in Europe and with localized large populations in northern Spain (Garbary et al., 2012 and references therein). Temperatures at or above 15°C may induce physiological stress (Werner & Dring, 2011; Morgan et al., 1980). In tank cultures of Palmaria palmata at 20°C and above, all plants were dead within a week (Morgan et al., 1980). Populations may be acclimated to typical conditions but it is likely that Palmaria palmata may be bleached or damaged by higher than usual temperatures.

Ulva spp. are characteristic of upper shore rock pools, where water and air temperatures are greatly elevated on hot days. Empirical evidence for thermal tolerance to anthropogenic increases in temperature is provided by the effects of heated effluents on rocky shore communities in Maine, USA. Ascophyllum and Fucus were eliminated from a rocky shore heated to 27-30°C by a power station whilst Ulva intestinalis (as Enteromorpha intestinalis) increased significantly near the outfall (Vadas et al., 1976).  

Sensitivity assessment.  Laminaria digitata is likely to withstand an increase in temperature at the benchmark level, some of the understorey of red algae, such as Palmaria palmata may be lost during acute temperature increases if these occur in the summer when plants are already close to the limit of thermal tolerances. Biotope resistance is assessed as 'High' and resilience as 'High' and the biotope is considered to be 'Not sensitive'. It should be noted that the timing of acute and chronic increases would alter the degree of impact and hence sensitivity.  An acute change occurring on the hottest days of the year and exceeding thermal tolerances may lead to mortality. 

Temperature decrease (local)

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

Evidence

Many intertidal species are tolerant of freezing conditions as they are exposed to extremes of low air temperatures during periods of emersion. They must also be able to cope with sharp temperature fluctuations over a short period of time during the tidal cycle. In winter, air temperatures are colder than the sea, conversely in summer air temperatures are much warmer than the sea. Species that occur in the intertidal are therefore generally adapted to tolerate a range of temperatures, with the width of the thermal niche positively correlated with the height of the shore (Davenport & Davenport, 2005). Local populations may be acclimated to the prevailing temperature regime and may therefore exhibit different tolerances to other populations subject to different salinity conditions and therefore caution should be used when inferring tolerances from populations in different regions.

The thermal optimum of Laminaria digitata is between 10-15°C, with reproductive ability impaired to 20% at 18°C (Arzel, 1998). Therefore while the current population may not be affected, recruitment may be reduced. Spore production only occurs between 5-10°C and is the most temperature sensitive stage of reproduction in Laminaria digitata. Outside this temperature range, reproduction is severely reduced and the species is at risk from local extinction in the short-term. In additional, a temperature increase to 22-23°C causes cell damage and death (Sundene, 1964; Bolton & Lüning, 1982). During an exceptionally warm summer in Norway, Sundene (1964) reported the destruction of Laminaria digitata plants exposed to temperatures of 22-23°C. The sensitivity of this species, therefore, relies on the current sea temperatures of the specific location (Bartsch et al., 2013). A minimum of 10 weeks a year between 5-18°C is needed in order to ensure spore formation and hence reproduction (Bartsch et al., 2013).

Lüning (1990) reported that Corallina officinalis from Helgoland survived 0°C when exposed for one week. New Zealand specimens were found to tolerate -4°C (Frazer et al., 1988). Lüning (1990) suggested that most littoral algal species were tolerant of cold and freezing. The associated species Mastocarpus stellatus has a broad geographical distribution (Guiry & Guiry, 2015) and throughout its range experiences wide variation in temperatures (although local populations may be acclimated to the prevailing thermal regime).  The photosynthetic rate of Mastocarpus stellatus higher on the shore fully recovered from 24 hrs at -20°C (Dudgeon et al., 1989). Photosynthesis in Mastocarpus stellatus also recovered quickly after experimental freezing (Dudgeon et al., 1989, 1995). Palmaria palmata does well in low temperatures, with an optimum between 6 and 15°C, consistent with a distribution in northern temperate and arctic waters. In the laboratory, plants only became fertile if left at temperatures between 5-7°C with a short light period (Van der Meer & Chen, 1979). Acute or chronic changes in temperature below 5°C may, therefore, reduce reproductive success although reproduction and vegetative growth in warmer months should compensate for any reduction in output. The green algae, Ulva spp. are eurytopic, found in a wide temperature range and in areas which frequently experience freezing conditions and are vulnerable to ice scour (Seed & Suchanek, 1992). 

Sensitivity assessment. The dominant kelp Laminaria digitata is thought to be a northern species and likely to retreat north as a result of climate change. Therefore, it is unlikely to be sensitive to a reduction in temperature at the benchmark level. Based on the characterizing and associated species, this biotope is considered to have ‘High’ resistance and ‘High' resilience (by default) to this pressure and is therefore considered to be ‘Not sensitive’. The timing of changes and seasonal weather could result in greater impacts on species. An acute decrease in temperature coinciding with unusually low winter temperatures may exceed thermal tolerances and lead to mortalities of the associated species, although this would not alter the character of the biotope.

Salinity increase (local)

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

Evidence

Local populations may be acclimated to the prevailing salinity regime and may, therefore, exhibit different tolerances to other populations subject to different salinity conditions and therefore caution should be used when inferring tolerances from populations in different regions.  This biotope is found in full (30-35 ppt) salinity (Connor et al., 2004). Biotopes found in the intertidal will naturally experience fluctuations in salinity where evaporation increases salinity and inputs of rainwater expose individuals to freshwater. Species found in the intertidal are therefore likely to have some form of behavioural or physiological adaptations to changes in salinity. 

Kelps are tolerant to short-term daily fluctuation in salinity and are recorded as tolerating 5-60 psu, however, they are much less tolerant to long-term changes with growth and photosynthetic rates declining either side of 20-45 psu (Gordillo et al., 2002; Karsten, 2007). Despite this tolerance, Laminaria digitata is considered to be a stenohaline species, and this biotope is only found in conditions of full salinity (Connor et al., 2004). Therefore, other species probably out-compete Laminaria digitata at the limits of its salinity tolerance, meaning that despite the biotope’s tolerance under conditions of no competition, under natural conditions this biotope is unlikely to occur in conditions above 40 psu.

The associated species are typically found in a range of salinities and tolerance of the red algae varied between species. Corallina officinalis is found in tide pools where salinities may fluctuate markedly during exposure to the air. Kinne (1971b) cites maximal growth rates for Corallina officinalis between 33 and 38 psu in Texan lagoons. Chondrus crispus is found in a range of salinities across its range and has been reported from sites with yearly salinity range 0-10 psu and 10-35 psu (Lindgren & Åberg, 1996) and sites from an average of 26-32  psu. However, at different salinities the ratio between the abundance of the tetrasporophyte phase and the gametophyte alters (Guidone & Grace, 2010).  Mathieson & Burns (1971) recorded maximum photosynthesis of Chondrus crispus in culture at 24 psu, but rates were comparable at 8, 16 and 32 psu. Photosynthesis continued up to 60 psu. Bird et al. (1979) recorded growth of Canadian Chondrus crispus in culture between 10 and 50 psu, with a maximum at 30 psu. Chondrus crispus would, therefore, appear to be euryhaline and tolerant of a range of salinities. Laboratory experiments have defined the upper and lethal lower limits for Palmaria palmata as 15 psu and 50 psu (Karsten et al., 2003), with optimal salinity defined as 23-34 psu (Robbins, 1978).

The associated Ulva species can survive hypersaline conditions in supralittoral rockpools subjected to evaporation and are considered to be a very euryhaline species, tolerant of extreme salinities ranging from 0 psu to 136 psu (Reed & Russell, 1979). Some variations in salinity tolerance between populations of Ulva intestinalis have been found, however, suggesting that plants have some adaptation to the local salinity regime (Alströem-Rapaport et al., 2010; Reed & Russell, 1979). Increased salinity is most likely to occur in the region of the littoral fringe and supralittoral zone and specimens from these areas were able to tolerate very high salinities, a significant decrease in regeneration only being recorded after exposure to concentrated seawater (102 psu and 136 psu) for >7 days (Reed & Russell, 1979). 

Sensitivity assessment. Little direct evidence was found to assess sensitivity to this pressure. Although some increases in salinity may be tolerated by the associated species present, these are generally short-term and mitigated during tidal inundation. This biotope is considered, based on distribution of Laminaria digitata and the associated red algal species on the mid to lower shore, to be sensitive to a persistent increase in salinity to > 40 ppt. Resistance is therefore assessed as ‘Low’ and recovery as ‘Medium’ (following restoration of usual salinity). Sensitivity is therefore 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

Local populations may be acclimated to the prevailing salinity regime and may therefore exhibit different tolerances to other populations subject to different salinity conditions and therefore caution should be used when inferring tolerances from populations in different regions. This biotope is found in full (30-35 ppt) salinity (Connor et al., 2004) and at the pressure benchmark a change to variable (18-35 ppt) or reduced (18-30 ppt) is considered. Biotopes found in the intertidal will naturally experience fluctuations in salinity where evaporation increases salinity and inputs of rainwater expose individuals to freshwater. Species found in the intertidal are therefore likely to have some form of behavioural or physiological adaptations to changes in salinity. 

Birkett et al. (1998b) suggested that kelps are stenohaline, in that they do not tolerate wide fluctuations in salinity and require regular salinities of 30-35 psu to maintain optimum growth rates. Growth rate may be adversely affected if the kelp plant is subjected to periodic salinity stress. Laminaria digitata tolerates a large salinity range within a 24 hour period (5-60 psu; Karsten, 2007).  At the extremes of this range, decreases in photosynthetic rates are evident, particularly at low salinities (Gordillo et al., 2002). In the study by Karsten (2007), kelp thalli were kept at constant salinities for 5 days, with their photosynthetic rates measured after 2 and 5 days. The lower salinity limit for Laminaria digitata lies between 10 and 15 psu. On the Norwegian coast, Sundene (1964) found healthy Laminaria digitata plants growing between 15 and 25 psu. Axelsson & Axelsson (1987) indicated damage of the plants’ plasma membranes occurs when salinity is below 20 or above 50 psu. Localized, long-term reductions in salinity to below 20 psu may result in the loss of kelp beds in affected areas (Birkett et al., 1998b).

Corallina officinalis is found in tide pools where salinities may fluctuate markedly during exposure to the air. Kinne (1971b) cites maximal growth rates for Corallina officinalis between 33 and 38 psu in Texan lagoons. Ulva species can survive hypersaline conditions in supralittoral rockpools subjected to evaporation and is considered to be a very euryhaline species, tolerant of extreme salinities ranging from 0 psu to 136 psu (Reed & Russell, 1979).

Edyvean & Ford (1984b) suggest that populations of Lithophyllum incrustans are affected by temperature changes and salinity and that temperature and salinity ‘shocks’ induce spawning but no information on thresholds was provided (Edyvean & Ford, 1984b). Populations of Lithophyllum incrustans were less stable in tide pools with a smaller volume of water that were more exposed to temperature and salinity changes due to lower buffering capacity. Sexual plants (or the spores that give rise to them) were suggested to be more susceptible than asexual plants to extremes of local environmental variables (temperature, salinity etc.) as they occur with greater frequency at sites where temperature and salinity were more stable (Edyvean & Ford, 1984b).

Laboratory experiments have defined the upper and lethal lower limits for Palmaria palmata as 15 psu and 50 psu (Karsten et al., 2003), with optimal salinity defined as 23-34 psu (Robbins, 1978). In-situ Palmaria palmata from the Arctic Kongsfjord (Spitsbergen) exposed for four days to salinities of 15 psu following freshwater run-off suffered high levels of mortality (Karsten et al., 2003). In Danish waters where salinities are lowered by freshwater inputs, cultivation experiments found that Palmaria palmata growth over a seven month period was greatest at a site where mean salinity was 21±3 psu, while no growth occurred at a site where mean salinity was 17±5 psu (Bak, 2014).

A decrease in salinity may lead to replacement of more sensitive red algal turf forming species by those more tolerant of the changed conditions. Chondrus crispus occurs in areas of 'low' salinity. For example, the species occurs in estuaries in New Hampshire, USA, where surface water salinity varies from 16-32 psu (Mathieson & Burns, 1975). Mathieson & Burns (1971) recorded maximum photosynthesis of Chondrus crispus in culture at 24 psu, but rates were comparable at 8, 16 and 32 psu. Tasende & Fraga (1999) cultured Chondrus crispus spores from north west Spain and concluded that growth was correlated with salinity between 23 and 33 psu. 

The associated Ulva species can survive hypersaline conditions in supralittoral rockpools subjected to evaporation and are considered to be a very euryhaline species, tolerant of extreme salinities ranging from 0 psu to 136 psu (Reed & Russell, 1979). Some variations in salinity tolerance between populations of Ulva intestinalis have been found, however, suggesting that plants have some adaptation to the local salinity regime (Alströem-Rapaport et al., 2010; Reed & Russell, 1979). Increased salinity is most likely to occur in the region of the littoral fringe and supralittoral zone and specimens from these areas were able to tolerate very high salinities, a significant decrease in regeneration only being recorded after exposure to concentrated seawater (102 psu and 136 psu) for >7 days (Reed & Russell, 1979).

Sensitivity assessment. Prolonged reduction in salinity, e.g. from full to reduced or variable, is likely to reduce the species richness of the biotope due to loss of less tolerant red algae and some intolerant invertebrates. The sensitivity of Palmaria palmata for example, appears to be greater than some other turf-forming species such as Chondrus crispus. A change in salinity at the pressure benchmark is considered to lead to some mortality of Palmaria palmata although the tolerance threshold reported in laboratory and cultivation studies is slightly lower than the assessed benchmark. Due to the variable or low salinity conditions the individual red seaweeds may not be as large as specimens found in fully marine conditions and they can lack sexually reproductive structures (JNCC, 2015). Based on changes in dominant species and reduction in habitat suitability for the characterizing species, biotope resistance is assessed as ‘Low’ and resilience as ‘Medium’ following habitat restoration. Biotope sensitivity is therefore ‘Medium’.

Water flow (tidal current) changes (local)

Benchmark. A change in peak mean spring bed flow velocity of between 0.1 m/s to 0.2 m/s for more than one year. Further detail

Evidence

This biotope occurs in a range of water flow conditions from moderately strong (0.5-1.5 meters /second) to weak (<0.5 m/s) (negligible) (Connor et al., 2004), indicating that the characterizing species can tolerate a range of flow speeds.Moderate water movement is beneficial to seaweeds as it carries a supply of nutrients and gases to the plants and removes waste products. Propagule dispersal, fertilization, settlement, and recruitment are also influenced by water movement (Pearson & Brawley, 1996). Increased water flow can increase scour through increased sediment movement. Small life stages of macroalgae are likely to be affected by removal of new recruits from the substratum reducing successful recruitment (Devinny & Volse, 1978) (see ‘siltation’ pressures).  A reduction in water flow can cause a thicker boundary layer resulting in lower absorption of nutrients and CO₂ by the macroalgae. Slower water movement can also cause oxygen deficiency directly impacting the fitness of algae (Olsenz, 2011). Higher water flow rates increase mechanical stress on macroalgae by increasing drag. This can result in individuals being torn off the substratum. 

In Lough Ine in Ireland, Laminaria digitata forms dense forests in the fast flowing water of the Rapids where water speeds vary from 4-6 knots (ca 2-3 m/s) (Bassindale et al., 1948). Laminaria digitata is also found in very strong flows (>3.87 m/s) although it is often out-competed by Alaria esculenta. Laminaria digitata partially achieves survival in a range of water flow conditions by variations in blade morphology, with fronds narrower and more digitate where water flow rates are higher (Sundene, 1964).  In a laboratory study, this morphological adaptation was attributed to longitudinal stress with exposure to this stress over 6 weeks resulting in narrower blades and a significantly higher rate of cell elongation, compared to those plants that had not experienced the same stress. This plasticity would serve to decrease the risk of thallus damage in areas of greater exposure or in stormier conditions (Gerard, 1987).

As water velocity increases, algae can flex and reconfigure to reduce the size of the alga when aligned with the direction of flow, this minimizes drag and hence the risk of dislodgement (Denny et al., 1998; Boller & Carrington, 2007). These characteristics allow these species to persist on shores that experience a range of flow speeds. For example, Mastocarpus stellatus occurs at sites in Maine, USA experiencing peak autumn flow speeds as measured by current meters of 9.2 m/s and 5.8 m/s. The habitat structure created by canopies and turfs reduce the effects of water flows on individuals by slowing and disrupting flow (Boller & Carrington, 2006), although this effect will be reduced in this biotope where Fucus serratus and red algae occur as scattered plants. The coralline crusts characterizing this biotope are securely attached and as these are flat are subject to little or no drag.

The crustose holdfasts of Corallina officinalis, the coralline crusts and the Mastocarpus stellatus petrocelis stage are securely attached and as these are relatively flat, are subject less drag than upright fronds and are likely to tolerate changes in water flows at the pressure benchmark. Moderate water movement is beneficial to seaweeds as it carries a supply of nutrients and gases to the plants and removes waste products. However, if flow becomes too strong, plants may become  dislodged.

Gibbula cineraria also appear to tolerate a range of wave exposures from exposed sites to those that are very sheltered (Frid & Fordham, 1994). As with Littorina littorea, the morphology of the shell varies  according to wave exposure, allowing individuals to adapt to different conditions in the habitat in which the larvae settle(Frid & Fordham, 1994). Gibbula cineraria is, however, absent from areas with very strong and turbulent flow

Sensitivity assessment.  Based on the available evidence the characterizing species and associated macroalgae and animals are able to occur within a range of flow flow rates and the biotope is therefore considered to be 'Not sensitive' to an increase in water flow at the pressure benchmark. A decrease in water flow may have some effects on recruitment and growth but this is not considered to be lethal at the pressure benchmark and resistance is therefore assessed as 'High' and resilience as 'High' by default, so that the biotope is considered to be 'Not sensitive'.  Changes in water flow at the pressure benchmark may result in increased or decreased sediment deposition, these are not considered to alter the character of the biotope which is characterized by sediments beneath boulders (Connor et al., 2004).

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

Emergence regime is a key factor structuring intertidal biotopes. Changes in emergence can lead to: greater exposure to desiccation, temperature and salinity variation, reduced levels of time for filter feeding and nutrient uptake, and photosynthesising opportunities for the characterizing species. Changes in emergence can also alter competitive interactions and trophic interactions such as grazing and predation. This biotope occurs in the lower shore beneath the Fucus serratus zone (Fser.Bo or Fser.R) and above the Laminaria hyperborea zone (Lhyp). Many of the animals found under boulders in the lower shore in Fser.Bo are also found under boulders in the sublittoral fringe (Ldig.Bo), particularly the sponges and crabs. Similarly, many of the seaweeds present on the lower shore are also present in the shallow sublittoral fringe (JNCC, 2015).

This biotope occurs in the shallow sublittoral and is therefore exposed to changes in emergence. Increased emergence will expose the biotope to air for longer periods leading to drying. Laminaria digitata is relatively resistant to desiccation, surviving up to 40% water loss (Dring & Brown, 1982).  The desiccation tolerance of Laminaria digitata allow beds to extend a further 2 cm into the eulittoral zone where grazing pressure is removed (Southward & Southward, 1978). When exposed to the air, kelp canopies buffer the effects of high temperatures and water loss on organisms below their fronds with substratum temperatures on average 8-10°C lower under the canopy than bare rock, additionally decreasing water loss by >45% (Bertness et al., 1999).

An increase in the benchmark level for air exposure may result in the depression of the biotope’s upper limit; as this species‘ lower limit is set by competition with Laminaria hyperborea (Hawkins & Harkin, 1985). The upper, landward limits of Laminaria digitata biotopes are generally set by competition with the brown algae Fucus serratus (Hawkins & Harkin, 1985). Therefore, a decrease in the benchmark level for air exposure may result in the extension of the biotope’s upper limit. The main driver of competition between Fucus serratus and Laminaria digitata is based on the ability of Fucus serratus to control its respiration rates based on its desiccation rates, which Laminaria digitata is unable to do. Therefore, longer periods of emergence may result in a compression of Laminaria digitata’s extent as it is out-competed by Fucus serratus at its upper limit. The kelp is able to resist both an increase and decrease in emergence, however, this resitance is based on the free movement of this species within its environmental optima, shifting up or down the shore. 

The red algae within the biotope are likely to be sensitive to increased emergence. Corallina officinalis is sensitive to desiccation (Dommasnes, 1969) and is generally not found on open rock unless protected by algal canopies or where the surfaces are damp or wet. At Hinkley Point (Somerset, England), for example, seawater run-off from deep pools high in the intertidal supports dense turfs of Corallina spp. lower on the shore (Bamber & Irving, 1993).  Fronds are highly intolerant of desiccation and do not recover from a 15% water loss, which might occur within 40-45 minutes during a spring tide in summer (Wiedemann, 1994). Bleached corallines were observed 15 months after the 1964 Alaska earthquake which elevated areas in Prince William Sound by 10 m. Similarly, increased exposure to air caused by upward movement of 15 cm due to nuclear tests at Armchitka Island, Alaska, adversely affected Corallina pilulifera (Johansen, 1974). During an unusually hot summer, Hawkins & Hartnoll (1985) observed damaged Corallina officinalis and other red algae. Littler & Kauker (1984) suggest that the basal crustose stage is adaptive, allowing individuals to survive periods of physical stress as well as physiological stress such as desiccation and heating. The basal crust stage may persist for extended periods with frond regrowth occurring when conditions are favourable.

Experimental grazer removal has allowed algae including Palmaria palmata, Ceramium sp. and Osmundea (as Laurencia) pinnatifida  to grow higher on the shore (during winter and damp summers) than usual, suggesting that grazing also limits the upper shore extent of this biotope (Hawkins & Hartnoll, 1985). These observations and further grazer removal experiments by Boaventura et al. (2003), indicate that grazing, in combination with physiological tolerances, limits the upper shore extent of biotopes characterized by red algal turfs on moderately and more exposed shores, where grazing is greater than on sheltered shores (Hawkins & Hartnoll, 1983; Boaventura et al., 2003).  These results concord with other studies that show grazing and emersion stress limit the height to which red algal turfs can extend (Underwood, 1980; Boaventura, 2000).

The green algae are considered resistant to this pressure (although may be bleached at higher shore levels during periods of high temperature) as they are found throughout the intertidal including the high shore levels which may not be inundated every day.

Sensitivity assessment. This pressure is a key driver of biotope extent because the upper and lower limits of this species are set by inter-species competition.  In the direct footprint of the impact resistance is therefore probably ‘Low’ based on loss of Laminaria digitata (loss of 25-75%) and likely reclassification to LR.MLR.BF.Fser.Bo.  Resilience is suggested as ‘High’ (2-10 years) following restoration of the emergence regime. This biotope is therefore considered to have ‘Medium’ sensitivity to the pressure.

Wave exposure changes (local)

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

Evidence

This biotope is found in a range of wave exposures from moderately exposed to sheltered from wave action (Connor et al., 2004).

An increase in wave exposure generally leads to a decrease in macroalgae abundance and size (Lewis, 1961; Stephenson & Stephenson, 1972; Hawkins et al., 1992; Jonsson et al., 2006).  The greatest wet weight of Laminaria digitata occurs at low wave exposure (mean significant wave height <0.4 m) decreasing by a mean of 83% in medium to high wave exposures (mean significant wave height >0.4m; Gorman et al., 2013).  At medium to high levels of wave exposure, Laminaria digitata biomass has been shown to decrease by 83% in the field (Wernberg & Thomsen, 2005). In areas of high wave exposure Laminaria digitata may extend its upper limits into the lower eulittoral zone.

As water velocity increases the algae can flex and reconfigure to reduce the size of the alga when aligned with the direction of flow, this minimises drag and hence the risk of dislodgement (Boller & Carrington, 2007). These characteristics allow these species to persist on shores that experience a range of wave action levels. Colonies of Lithophyllum incrustans appear to thrive in conditions exposed to strong water movement. Irvine & Chamberlain (1994) observe that the species is best developed on wave exposed shores. 

Sensitivity assessment.  The natural wave exposure range of this biotope is considered to exceed changes (increases and decreases) at the pressure benchmark and this biotope is considered to have 'High' resistance and 'High' resilience (by default), to this pressure (at the benchmark).  This assessment is supported by evidence for the tolerance and adaptions of the key characterizing macroalgae to different levels of wave exposure. 

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.

Little information was found concerning the effects of heavy metals on turf forming and encrusting coralline algae. However, Bryan (1984) suggested that the general order for heavy metal toxicity in seaweeds is: organic Hg >inorganic Hg >Cu >Ag >Zn >Cd >Pb.

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.

Laminaria digitata is less susceptible to coating than some other seaweeds because of its preference for exposed locations where wave action will rapidly dissipate oil. The effects of oil accumulation on the thalli are mitigated by the perennial growth of kelps. No significant effects of the Amoco Cadiz spill were observed for Laminaria populations and the World Prodigy spill of 922 tons of oil in Narragansett Bay had no discernible effects on Laminaria digitata (Peckol et al., 1990). Mesocosm studies in Norwegian waters showed that chronic low level oil pollution (25 µg/l) reduced growth rates in Laminaria digitata but only in the second and third years of growth (Bokn, 1985). Where exposed to direct contact with fresh hydrocarbons, encrusting calcareous algae have a high intolerance. The sensitivities of the faunal components of the kelp bed are not known although amphipods normally suffer high mortality in oil affected areas. Analysis of kelp holdfast fauna after the Sea Empress oil spill in Milford Haven illustrated decreases in number of species, diversity and abundance at sites nearest the spill (SEEEC, 1998).

Following the Torrey Canyon oil spill in 1967, oil and detergent dispersants affected high shore specimens of Corallina officinalis more than low shore specimens. Plants in deep pools were afforded some initial protection, although probably later affected by contaminated runoff. In areas of heavy spraying, however, Corallina officinalis was killed (Smith, 1968). Intolerance to hydrocarbon pollution has been assessed to be high, as key structural and important characterizing coralline algal species will be lost and the biotope not be recognized in their absence. Hydrocarbon contamination, at levels greater than the benchmark, e.g. from spills of fresh crude oil or petroleum products, may cause significant loss of Ulva spp. However, the species tends to recover very rapidly from oil pollution incidents. For instance, after the Torrey Canyon tanker oil in 1967, grazing species were killed, and a dense flush of ephemeral green algae (Ulva, Blidingia) appeared on the rocky shore within a few weeks and persisted for up to one year (Smith, 1968).

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.

Cole et al. (1999) suggested that herbicides were (not surprisingly) very toxic to algae and macrophytes. Hoare & Hiscock (1974) noted that with the exception of Phyllophora species, all red algae including encrusting coralline forms, were excluded from the vicinity of an acidified halogenated effluent discharge in Amlwch Bay, Anglesey, and that intertidal populations of Corallina officinalis occurred in significant amounts only 600 m east of the effluent. Chamberlain (1996) observed that although Lithophyllum incrustans was quickly affected by oil during the Sea Empress spill, recovery occurred within about a year. The oil was found to have destroyed about one third of the thallus thickness but regeneration occurred from thallus filaments below the damaged area.

Following the Torrey Canyon oil spill in 1967, oil and detergent dispersants affected high shore specimens of Corallina officinalis more than low shore specimens. Plants in deep pools were afforded some initial protection, although probably later affected by contaminated runoff. In areas of heavy spraying, however, Corallina officinalis was killed (Smith 1968). Limpets are extremely intolerant of aromatic solvent based dispersants used in oil spill clean-up. During the clean-up response to the Torrey Canyon oil spill nearly all the limpets were killed in areas close to dispersant spraying. Viscous oil will not be readily drawn in under the edge of the shell by ciliary currents in the mantle cavity, whereas detergent, alone or diluted in seawater, would creep in much more readily and be liable to kill the limpet (Smith, 1968). A concentration of 5 ppm killed half the limpets tested in 24 hours (Southward & Southward, 1978; Hawkins & Southward, 1992). Acidified seawater affects the motility of Patella vulgata. At a pH of 5.5, motility was reduced whilst submerged but individuals recovered when returned to normal seawater. At a pH of 2.5, total inhibition of movement occurred and when returned to normal seawater half had died (Bonner et al., 1993). Reduced motility reduces time for foraging and may result in decreased survival of individuals. Acidified seawater can also change the shell composition which will lead to a decrease in its protective nature and hence survival (Bonner et al., 1993). Short periods (48 hours) are unlikely to have much effect on a population but long periods (1 year) may cause reduced grazing and an increase in algal growth. However, seawater is unlikely to reach pH 2.5 therefore intolerance to slight changes in pH will be low. Hoare & Hiscock (1974) reported that in Amlwch Bay, Patella vulgata was excluded from sites within 100-150 m of the discharge of acidified, halogenated effluent.

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.

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 inhibit 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).

This biotope would only be exposed to low oxygen in the water column during periods of tidal immersion. In areas of wave exposure and/or moderately strong current flow, low oxygen levels in the water are unlikely to persist for very long as oxygen levels will be recharged by the incorporation of oxygen in the air into the water column or flushing with oxygenated waters.  

Reduced oxygen concentrations have been shown to inhibit 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). 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). 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.

Experiments have shown that thallus discs of Ulva lactuca plants can survive prolonged exposure to anoxia and hypoxia (Vermaat & Sand-Jensen, 1987; Corradi et al., 2006). Following resumption of normal oxygen conditions gametes were produced. The associated invertebrate species also show high tolerances for reduced oxygen at levels that exceed the pressure benchmark. Littorina littorea can easily survive 3-6 days of anoxia (Storey et al., 2013). Semibalanus balanoides can respire anaerobically, so they can tolerate some reduction in oxygen concentration (Newell, 1979). When placed in wet nitrogen, where oxygen stress is maximal and desiccation stress is low, Semibalanus balanoides have a mean survival time of 5 days (Barnes et al., 1963). Limpets can also survive for a short time in anoxic seawater; Grenon & Walker (1981) found that in oxygen free water limpets could survive up to 36 hours, although Marshall & McQuaid (1989) found a lower tolerance for Patella granularis, which survived up to 11 hours in anoxic water. Patella vulgata and Littorina littorea are able to respire in air, mitigating the effects of this pressure during the tidal cycle.

Sensitivity assessment. As the biotope will only be exposed to this pressure when submerged during the tidal cycle and wave action will re-oxygenate waters while respiration will occur in air, biotope resistance was assessed as ‘High’ and resilience as ‘High’ (no effect to recover from), resulting in a sensitivity of 'Not sensitive'.   

Nutrient enrichment

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

Evidence

This pressure relates to increased levels of nitrogen, phosphorus and silicon in the marine environment compared to background concentrations. The benchmark is set at compliance with WFD criteria for good status, based on nitrogen concentration (UKTAG, 2014).  

High levels of enrichment may stimulate algal blooms and macroalgal growth. Stimulation of fast-growing green algae may result in smothering of boulder surfaces and lead to negative effects on both perennial algae and bases and the characterizing invertebrate hinder perennial species development or harm their recruitment. High ambient levels of phosphate and nitrogen enhance spore formation in a number of Laminaria species (Nimura et al., 2002), but will eventually inhibit spore production, particularly at the limits of temperature tolerances as seen in Saccharina latissima (studied as Laminaria saccharina; Yarish et al., 1990). Laminaria digitata seems to follow this trend with a growth peak occurring in conjunction with nutrient upwelling from deeper waters in Norway (Gévaert et al., 2001). Macroalgal growth is generally nitrogen-limited in the summer, as illustrated by the growth rates of Laminaria digitata between an oligotrophic and a eutrophic site in Abroath, Scotland (Davison et al., 1984). Laminaria digitata does not accumulate the significant internal nutrient reserves seen in some other kelp. Higher growth rates have been associated with alga situated close to sewage outfalls. However, after removal of sewage pollution in the Firth of Forth, Laminaria digitata became abundant on rocky shores from which they had previously been absent (Read et al., 1983). Enhancement of coastal nutrients is likely to favour those species with more rapid growth rates including turf forming algae (Gorgula & Connell, 2004) which could explain Laminaria digitata absence from the Firth of Forth. Additionally, epiphytic abundance and biomass on Laminaria longicruris increases under a eutrophic regime decreasing the ability to photosynthesis and withstand pressure from water movement as drag increases (Scheibling et al., 1999).

The red alga Corallina officinalis and the associated green algae species have been identified worldwide as species that occur in areas subject to increased nutrient input within the vicinity of sewage outfalls and at intermediately polluted sites (Bellgrove et al., 2010; Littler & Murray, 1975; May, 1985; Brown et al., 1990; Bellgrove et al., 1997). For example, Kindig & Littler (1980) demonstrated that Corallina officinalis var. chilensis in South California showed equivalent or enhanced health indices, highest productivity and lowest mortalities (amongst the species examined) when exposed to primary or secondary sewage effluent. Grazers in the biotope may also benefit from increased availability of food resources, due to enhanced growth.

Atalah & Crowe (2010) added nutrients to rockpools occupied by a range of algae including encrusting corallines, turfs of Mastocarpus stellatus, Chondrus crispus and Corallina officinalis and green and red filamentous algae. The invertebrates present were mostly Patella ulyssiponensis, the winkle Littorina littorea and the flat topshell Gibbula umbilicalis. Nitrogen and phosphorous enhancement was via the addition of fertilizers, as either 40 g/l or 20 g/l. The treatments were applied for seven month and experimental conditions were maintained every two weeks. The experimental treatments do not directly relate to the pressure benchmark but indicate some general trends in sensitivity. Nutrients had no significant effect on the cover of Corallina officinalis. The cover of green filamentous algae was significantly increased both by reduced grazing and increased nutrients, although the effect size was synergistically magnified by the combined effect of grazer removal and nutrients. Nutrient enrichment caused an absolute increase in the average cover of green filamentous algae of 19% (±3.9 S.E.) respect to the control treatments while the cover of red turfing algae was not affected by nutrient addition (Atalah & Crowe, 2010).

Sensitivity assessment. The pressure benchmark is relatively protective and may represent a reduced level of nutrient enrichment in previously polluted areas. Due to the tolerance of high levels of nutrient input demonstrated generally by red algae, including Corallina officinalis e.g. Bellgrove et al. (2010) and Atalah & Crowe (2010), resistance to this pressure is assessed as ‘High’ and resilience as ‘High’ so that the biotope is assessed as ‘Not sensitive’. Grazers limit the effects of nutrient enrichment; in the absence of Gibbula cineraria and other grazers, significant changes in the structure of the algal assemblage could emerge following eutrophication. However, where boulders move frequently this would prevent permanent colonization by larger, perennial species and ephemeral algae could be displaced by space-occupying red algae following disturbance and the creation of gaps.

Organic enrichment

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

Evidence

It should be noted that biotopes occurring in tide swept or wave exposed areas are less likely to experience the effects of organic enrichment as the organic matter will be rapidly removed. Organic matter may be moved to the sediments beneath the boulders and would enhance food supply to deposit feeding infauna such as Cirratuls cirratulus, other polychaetes and oligochaetes. At the pressure benchmark, the input of organic carbon would represent a food subsidy leading to enrichment rather than gross pollution effects.

Organic enrichment and nutrient enrichment commonly co-occur, for example sewage deposits or outputs from fish farms may enhance nitrogen and phosphorous and organic matter. Nutrient enrichment alters the selective environment by favouring fast growing, ephemeral species such as Ulva lactuca and Ulva intestinalis (Berger et al., 2004; Kraufvelin, 2007). Rohde et al. (2008) found that both free growing filamentous algae and epiphytic microalgae can increase in abundance with nutrient enrichment. This stimulation of annual ephemerals may accentuate the competition for light and space and hinder perennial species development or harm their recruitment (Berger et al., 2003; Kraufvelin et al., 2007). Bellgrove et al. (2010) found that coralline turfs out-competed fucoids at a site associated with organic enrichment caused by an ocean sewage outfall. Worldwide Corallina officinalis has been noted to increaseat the expense of canopy forming macroalgae within the vicinity of sewage outfalls and at intermediately polluted sites (Bellgrove et al., 2010; Littler & Murray, 1975; May, 1985; Brown et al., 1990). As turf forming algae Corallina spp. trap large amounts of sediment and are therefore not considered sensitive to sedimentation. The turfs host a variety of associated species and deposit feeders amongst these would be able to consume inputs of organic matter.

Sensitivity assessment. Evidence is limited but it is considered that this biotope has ’High’ resistance to increased organic matter at the pressure benchmark (which represents enrichment rather than gross pollution). Resilience is therefore assessed as ‘High’ (no effect to recover from) and the biotope is considered to be 'Not sensitive'.

Physical loss (to land or freshwater habitat)

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

Evidence

All marine habitats and benthic species are considered to have a resistance of ‘None’ to this pressure and to be unable to recover from a permanent loss of habitat (resilience is ‘Very Low’). Sensitivity within the direct spatial footprint of this pressure is therefore ‘High’. Although no specific evidence is described, confidence in this assessment is ‘High’ due to the incontrovertible nature of this pressure.  Adjacent habitats and species populations may be indirectly affected where meta-population dynamics and trophic networks are disrupted and where the flow of resources e.g. sediments, prey items, loss of nursery habitat etc. is altered.

Physical change (to another seabed type)

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

Evidence

This biotope is characterized by the hard rock substratum, provided by the boulders, to which the characterizing Laminaria digitata and associated species such as red and green algae, barnacles and sponges can firmly attach. A change to a sedimentary substratum (without boulders) would significantly alter the character of the biotope through the loss of boulders and associated changes to the sedimentary assemblage.  A biological assemblage more typical of the changed conditions would develop. A change to an artificial hard substratum could alter this biotope as it would not be equivalent to a boulder field on sediments. 

Artificial hard substratum may also differ in other characteristics from natural hard substratum, so that replacement of natural surfaces with artificial may lead to changes in the biotope through changes in disturbance (Sousa, 1979), microhabitat provision (McGuinness & Underwood, 1986), changes in species composition, richness and diversity (Green et al., 2012; Firth et al., 2014) or the presence of non-native species (Bulleri & Airoldi, 2005). 

Tests  with stone panels  fixed to the sublittoral, mid-tide and high-tide levels of varying roughness found that Ulva species settle preferentially on smother, fine grained, substratum (chalk, mottled sandstone) and Porphyra purpurea on rougher, granulated substratum (limestone, granite, basaltic larvae) (Luther, 1976).  Corallina officinalis shows optimal settlement on finely rough artificial substrata (0.5 - 1 mm surface particle diameter). Although spores will settle and develop as crustose bases on smooth surfaces, fronds were only initiated on rough surfaces. Corallina officinalis settled on artificial substrata within one week in the field in summer months in New England (Harlin & Lindbergh 1977). Crustose coralline algae extend further to the undersides of natural, rounded boulders than experimental stone blocks (Liversage, 2015). This pattern is likely due to availability of light (Liversage, 2015).  

Sensitivity assessment. A change to a soft sedimentary or artificial, stable hard substratum would remove the habitat for this biotope. Biotope resistance is assessed as ‘None’ and resilience as ‘Very Low’ as the change is considered to be permanent. Sensitivity is therefore assessed as 'High'.

Physical change (to another sediment type)

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

Evidence

A change in sediment type below the boulders would be very likely to alter the biological assemblage as soft sediment infauna are highly sensitive to changes in sediment type. Changes in the size and shape and other characteristics of boulders would also lead to changes in the habitat. Boulders provide three microhabitats, the upper and lower surface of boulders and the substratum underneath the boulders (Cruz Motta et al., 2003).

Sensitivity assessment. A change in boulder and sediment characteristics are likely to lead to changes in species composition, and shifts in abundance and distribution of species that remain. The biotope classification is unlikely to change while the species composition is relatively similar. Biotope resistance is assessed as ‘Low’ and resilience is Very low (the pressure is a permanent change), biotope 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

Removal of boulders would result in loss of this habitat. Biotope resistance is assessed as ‘None’ and resilience as ‘Medium’ following restoration of the habitat. Sensitivity is, therefore, assessed as 'Medium'.

Abrasion / disturbance of the surface of the substratum or seabed

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

Evidence

The species characterizing this biotope occur on the rock and therefore have no shelter from abrasion at the surface.

Most macroalgae are very flexible but not physically robust. Brown algae are particularly intolerant of trampling, depending on intensity. Fucoid algae demonstrate a rapid (days to months) detrimental response to the effects of trampling, depending on species, which has been attributed to either the breakage of their fronds across rock surfaces (Boalch et al., 1974) or their possession of small discoid holdfasts that offer little resistance to repeated impacts (Brosnan & Crumrine, 1992; Fletcher & Frid, 1996b). Foliose species such as Mastocarpus spp. are also likely to be intolerant of trampling (Brosnan & Crumrine, 1994). Brosnan (1993) suggested that the presence or absence of foliose algae (e.g. fucoids) could be used to indicate the level of trampling on the rocky shores of Oregon. 

In the UK, Boalch et al. (1974) and Boalch & Jephson (1981) noted a reduction in the cover of fucoids at Wembury, south Devon, when compared to surveys conducted by Colman (1933). The size ranges of Ascophyllum nodosum, Fucus vesiculosus and Fucus serratus were skewed to smaller length, and the abundance of Ascophyllum nodosum in particular was reduced (Boalch & Jephson, 1981). It was suggested that visitor pressure, especially after the construction of a car park, was responsible for the reduced cover of fucoids (Boalch et al., 1974). They suggested that the raised edges of the slatey rock severed fronds when the rocks were walked over. However, no quantitative data was provided. Conversely, algal turfs seem to be relatively tolerant of the direct effects of trampling (based on the available evidence) and some species may benefit from removal of canopy forming algae (Tyler-Walters, 2005). Their tolerance may result from their growth form as has been shown for vascular plants and corals (Liddle, 1997). Brosnan (1993) suggested that algal turf dominated areas (on shores usually dominated by fucoids) were indicative of trampling on the rocky shores of Oregon. However, tolerance is likely to vary with species and their growth form and little species specific data was found. Furthermore, algal turfs may suffer negative indirect effects where they form an understorey below canopy forming species. 

Pinn & Rodgers (2005) compared a heavily visited ledge with a less visited ledge at Kimmeridge Bay, Dorset. Although the mean species richness was similar at both sites, the total number of species was greater at the less utilized site.  Comparatively, the heavily utilized ledge displayed a reduction in larger, branching algal species (e.g. Fucus serratus) and increased abundances of ephemeral and crustose species (e.g. Ulva linza and Lithothamnia spp. respectively). Fletcher & Frid (1996a, 1996b) examined the effects of persistent trampling on two sites on the north east coast of England. The trampling treatments used were 0, 20, 80, and 160 steps per m² per spring tide for 8 months between March and November. Using multivariate analysis, they noted that changes in the community dominated by fucoids (Fucus vesiculosus, Fucus spiralis and Fucus serratus) could be detected within 1 to 4 months of trampling, depending on intensity. Intensive trampling (160 steps/m²/spring tide) resulted in a decrease in species richness at one site. The area of bare substratum also increased within the first two months of trampling but declined afterwards, although bare space was consistently most abundant in plots subject to the greatest trampling (Fletcher & Frid, 1996a, 1996b). The abundance of fucoids was consistently lower in trampled plots than in untrampled plots. 

Fletcher & Frid (1996a, 1996b) also reported a decrease in the understorey algal community of encrusting coralline algae and red algae, which was probably an indirect effect due to increased desiccation after removal of the normally protective fucoid canopy (see Hawkins & Harkin, 1985) by trampling. They also noted that opportunistic algae (e.g. Ulva sp.) increased in abundance. Fletcher & Frid (1996a) noted that the species composition of the algal community was changed by as little as 20 steps per m² per spring tide of continuous trampling since recolonization could not occur. A trampling intensity of 20 steps per m² per spring tide could be exceeded by only five visitors taking the same route out and back again across the rocky shore in each spring tide. Both of the sites studied receive hundreds of visitors per year and damage is generally visible as existing pathways, which are sustained by continuous use (Fletcher & Frid, 1996a, 1996b). However, the impact was greatest at the site with the lower original abundance of fucoids.

Brosnan & Crumrine (1994) noted that trampling significantly reduced algal cover within 1 month of trampling. Foliose algae were particularly affected and decreased in cover from 75% to 9.1% in trampled plots. Mastocarpus papillatus decreased in abundance from 9% to 1% in trampled plots but increased in control plots. Fucus distichus decreased in the summer months only to recover in winter but in trampled plots remained in low abundance (between 1 and 3% cover). Trampling resulted in a decrease in cover of Pelvetiopsis limitata from 16% to 1.5%. Iridaea cornucopiae decreased from 38 to 14% cover within a month and continued to decline to 4-8% cover. However, after trampling ceased, recovery of algal cover including Iridaea cornucopiae and Mastocarpus papillatus was rapid (ca 12 months) (Brosnan & Crumrine, 1994). Schiel & Taylor (1999) also observed a decrease in understorey algae (erect and encrusting corallines) after 25 or more tramples, probably due to an indirect effect of increased desiccation as above. However, Schiel & Taylor (1999) did not detect any variation in other algal species due to trampling effects. Similarly, Keough & Quinn (1998) did not detect any effect of trampling on algal turf species. Littler & Littler (1984) suggest that the basal crustose stage of Corallina officinalis is adaptive to resist sand scour and wave shearing (as well as physiological stressors such as desiccation and heating). The base is much tougher than the fronds shown by experiments that demonstrate that the base has nearly twice the mechanical resistance (measured by penetration) of fronds (Littler & Kauker, 1984). In general, studies show that Corallina and other turf forming algae appear to be relatively resistant to single events and low levels of trampling.  Brosnan & Crumrine (1994), for example, found that in experimentally trampled plots the cover of foliose and canopy forming species declined while turf forming algae were relatively resistant. Similarly, a comparison of rocky intertidal ledges that received different amounts of visitors in Dorset, England, found that Corallina officinalis were present on both heavily visited and less visited ledges suggesting that this species has some resistance to trampling (Pinn & Rodgers, 2005).  Povey & Keough (1991) in Mornington Peninsula, Australia, investigated the effects of sustained trampling on intertidal coralline algal mats where upright branching Corallina spp. formed a turf with other red algae with sand and encrusting coralline algae between turfs.  The experimental strips were 2 m long and 0.5 m wide. The percentage cover of upright Corallina spp. was significantly affected by 25 passages of a strip per day after 12 and 33 days. The algae appeared flattened and were shorter (1-2 cm high) compared with the low intensity and control plots (3-4 cm high). However, low intensity trampling within a strip (2 passages/day) did not significantly affect the coralline turf. Brown & Taylor (1999) found that higher intensities of trampling damaged turfs. Moderate (50 steps per 0.09 m²) or more trampling on intertidal articulated coralline algal turf in New Zealand reduced turf height by up to 50%, and weight of sand trapped within turf to about one third of controls. This resulted in declines in densities of the meiofaunal community within two days of trampling. Although the community returned to normal levels within 3 months of trampling events, it was suggested that the turf would take longer to recover its previous cover (Brown & Taylor, 1999). Similarly, Schiel & Taylor (1999) noted that trampling had a direct detrimental effect on coralline turf species on the New Zealand rocky shore. At one site coralline bases were seen to peel from the rocks (Schiel & Taylor, 1999), however, this was probably due to increased desiccation caused by loss of the algal canopy.

Schiel & Taylor (1999) reported the death of encrusting corallines one month after trampling due to removal of their protective canopy of fucoids by trampling (10 -200 tramples where one trample equals one transect walked by one person). A higher proportion of corallines died back in spring treatments presumably due to the higher levels of desiccation stress expected at this time of year. However, encrusting corallines increased within the following year and cover returned to control levels within 21 months (Schiel & Taylor, 1999). Mechanical abrasion from scuba divers was also reported to impact encrusting corallines, with cover of Lithophyllum stictaeforme greater in areas where diving was forbidden than visited areas (abundance, 6.36 vs 1.4; it is presumed this refers to proportion of cover, although this is not clear from the text) (Guarinieri et al., 2012).

Dethier (1994) experimentally manipulated surface abrasion on a range of encrusting algae including Lithophyllum impressum. Crusts were brushed with either a nylon or steel brush for 1 minute a month for 24 months. Unbrushed controls grew by approximately 50% where the cover of nylon brushed crusts and steel brushed crusts decreased by approximately 25% and 40% respectively (interpreted from figures in Dethier, 1994). In laboratory tests on chips of Lithophyllum impressum brushing with a steel brush for 1 minute once a week for 3 weeks, resulted in no cover loss of two samples while a third ‘thinned and declined’ (Dethier, 1994).

Ulva spp. fronds are very thin and could be torn and damaged and individuals may be removed from the substratum, altering the biotope through changes in abundance and biomass. Ulva spp. cannot repair damage or reattach but torn fronds could still photosynthesize and produce gametes. Tearing and cutting of the fronds has been shown to stimulate gamete production and damaged plants would still be able to grow and reproduce. 

The effects of trampling on barnacles appears to be variable with some studies not detecting significant differences between trampled and controlled areas (Tyler-Walters & Arnold, 2008). However, this variability may be related to differences in trampling intensities and abundance of populations studied. The worst case incidence was reported by Brosnan & Crumrine (1994) who found that a trampling pressure of 250 steps in a 20x20 cm plot one day a month for a period of a year significantly reduced barnacle cover (Semibalanus glandula and Chthamalus dalli) at two study sites. Barnacle cover reduced from 66% to 7% cover in 4 months at one site and from 21% to 5% within 6 months at the second site. Overall barnacles were crushed and removed by trampling. Barnacle cover remained low until recruitment the following spring. Long et al. (2011) also found that heavy trampling (70 humans /km/hrs) led to reductions in barnacle cover. Single step experiments provide a clearer, quantitative indication of sensitivity to single events of direct abrasion. Povey & Keough (1991) in experiments on shores in Mornington peninsula, Victoria, Australia, found that in single step experiments 10 out of 67 barnacles (Chthamlus antennatus about 3 mm long) were crushed.

Sensitivity assessment. The available evidence indicates that abrasion could cause a significant loss of macroalgae cover and a reduction in species abundance and diversity. Based on the available evidence, it is concluded that the biotope is sensitive to abrasion and that resistance of characterizing and associated species (excluding Corallina officinalis) is ‘Low’ (loss of 25-75% of bed within direct impact footprint), resilience is assessed as ’Medium', resulting in a sensitivity of ‘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

Disturbance that leads to movement and overturning of boulders is a key factor structuring the community. Disturbance can affect species numbers under boulders (McGuiness, 1987). Disturbance can also affect the pattern of algal cover on boulders (Addessi, 1994) and overturning is a key factor in determining species richness (Sousa, 1979). Boulders that are subject to high levels of disturbance and over-turning are colonized by fast growing green algae and disturbance resistance species while large boulders that are rarely over-turned host late successional communities (Sousa, 1979). The biotope IR.MIR.KR.Ldig.Bo as described (Connor et al., 2004), is species rich and is unlikely to be subject to frequent disturbance. A single event of overturning, where the upper surface is turned on to the sediment is likely to lead to loss of algae as these will be smothered and damage and mortality of attached epifauna. Some under-boulder species such as amphipods and polychaetes may be able to relocate back to the underside of the boulder.

Sensitivity assessment. A single event of disturbance leading to the boulder being overturned is likely to alter species composition. Biotope resistance is assessed as ‘Low' and resilience as ‘Medium’, biotope sensitivity is therefore ‘Medium’.

Changes in suspended solids (water clarity)

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

Evidence

Intertidal biotopes will only be exposed to this pressure when submerged during the tidal cycle and thus have limited exposure. Siltation, which may be associated with increased suspended solids and the subsequent deposition of these is assessed separately (see siltation pressures). In general, increased suspended particles reduce light penetration and increase scour and deposition. Changes in suspended solids may enhance food supply to filter or deposit feeders (where the particles are organic in origin) or decrease feeding efficiency (where the particles are inorganic and require greater filtration efforts). The deposit feeding infauna, such as Cirratulus cirratulus, that are present in the sediment below boulders and in trapped sediments amongst the algae are not likely to be directly sensitive to increased or decreased turbidity.

Light availability and water turbidity are principal factors in determining depth range at which kelp can be found (Birkett et al., 1998b), an increase in suspended solids and decrease in light penetration is, therefore, directly relevant to this biotope. 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 1 percent 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 kelp is found may be reduced, or in some cases excluded completely (e.g. Severn Estuary), because of the alteration in light attenuation by suspended sediment (Lüning, 1990; Birkett et al., 1998b). The absence of Laminaria digitata in the Firth of Forth was suggested to be caused by the outflow from a sewage treatment plant that increased the turbidity of the water and thus decreased photosynthetic activity, although the effect of turbidity was probably coupled with increased nutrient levels (Read et al., 1983). Blue light is crucial for the gametophytic stages of Laminaria digitata, and several other congenic species (Lüning, 1980).  Dissolved organic materials (yellow substance or gelbstoff) absorbs blue light (Kirk, 1976), therefore changes in riverine input or other land based runoff are likely to influence kelp density and distribution.  In the silt-laden waters around Helgoland, Germany, the depth limit for Laminaria digitata growth may be reduced to between 0 m and 1.5 m (Birkett et al., 1998b). In locations where water clarity is severely decreased, Laminaria species experience a significant decrease in growth from the shading of suspended matter and/or phytoplankton (Lyngby & Mortensen, 1996; Spilmont et al., 2009).

Increases in the cover of sediment trapping, turf forming red algae at the expense of canopy forming species has been observed worldwide in temperate systems and has been linked to increased suspended solids linked to human activities worldwide (Airoldi, 2003). As turfs of Osmundea pinnatifida trap sediments (Prathep et al., 2003), it is clear that this species has some resistance to abrasion and scour from sediment particles.  Corallina species accumulate more sediment than any other alga (Hicks, 1985). Hence an increase in suspended sediment is likely to accumulate in the patches of Corallina officinalis. A significant increase may result in smothering (see siltation pressures). An accumulation of sediment within the turf may attract more sediment dwelling interstitial invertebrates such as nematodes, harpacticoids and polychaetes, although in more wave exposed locations accumulation of sediment is likely to be minimal. Increased suspended sediment may also result in increased scour, which may adversely affect Fucus vesiculosus and foliose red algae, and interfere with settling spores and recruitment if the factor is coincident with their major reproductive period. However, coralline algae, especially the crustose forms are thought to be resistant of sediment scour (Littler & Kauker, 1984), and will probably not be adversely affected at the benchmark level.

The biotope occurs in shallow waters where light attenuation due to increases in turbidity is probably low. Red algae and coralline algae especially are known to be shade tolerant and are common components of the understorey on seaweed dominated shores. Limited shading from suspended sediments is therefore not considered to negatively affect this genus. Palmaria palmata is often found under partially shaded conditions as an epiphyte on the stems of Laminaria spp. (Morgan et al. 1980) in the sublittoral zone (Lüning, 1990). In the Bay of Fundy where the tidal flux of nutrients from the marshes includes a high level of suspended sediment, Palmaria palmata grows well despite high turbidity. Irvine (1983) observed morphological adaptation of the plant in fairly sheltered, silty conditions; sometimes the blade divisions are wedge-shaped and finely dissected above or the blade has numerous linear divisions throughout. It is likely that this form reduces possible smothering that may result from increased siltation resulting from increased levels of suspended sediments. In the absence of nutrients, short-term increase in turbidity may affect growth and reproduction, however, as a perennial, the adults will probably survive. Other red algal species have high tolerances for high levels of suspended solids. Chondrus crispus occurs in areas of sand covered rock in the subtidal biotope IR.HIR.Ksed.ProtAhn suggesting it is very resistant to high levels of turbidity and scour associated with high levels of resuspended particles.

On sites affected by high levels of resuspended colliery waste particles, Hyslop et al. (1997) found that Palmaria palmata and Ulva spp. Were reduced or absent, although the more tough fucoids were less affected. It is not clear how the levels of suspended solids experienced by these sites relate to the pressure benchmark.

Experiments have shown that Ulva is a shade tolerant genus and can compensate for reduced irradiance by increasing chlorophyll concentration and light absorption at low light levels. Ulva spp. Were able to survive over two months in darkness and to begin photosynthesising immediately when returned to the light (Vermaat & Sand-Jensen, 1987). Limited shading from suspended sediments is therefore not considered to negatively affect this genus.

Sensitivity assessment. The exposure of this biotope to suspended sediments in the water column will be limited to immersion periods, and wave action will reduce accumulation.  The biotope is considered to be ‘Not sensitive’ to a reduction in suspended solids, although this may reduce food supply to  barnacles and other filter and deposit feeders that occur in this biotope. An increase in suspended solids may lead to some sub-lethal abrasion of fronds and some reduction in photosynthesis while submerged with some effects on recruitment. Evidence globally indicates that increase suspended solids favour the turf-forming algae that occur within this biotope (Airoldi, 2003). Resistance is therefore assessed as ‘Low’ and resilience as ‘High’ so that sensitivity of the biotope is considered to be ‘Low’. An increase in suspended solids above the pressure benchmark may result in a change in species composition with an increase in species seen in very turbid, silty environments e.g. Ahnfeltia plicata, Rhodothamniella floridula, Polyides rotunda and Furcellaria lumbricalis.

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

Sedimentation can directly affect assemblages inhabiting rocky shores in different ways, but the main direct effects are burial/smothering and scour/abrasion of organisms. The degree of smothering experienced by the characterizing species will be influenced by the size and shape of the boulders. In areas with greater water flow or wave action, excess sediments will be removed from the rock surface within a few tidal cycles and may be redeposited on the sediments below the boulders, although scour patterns around boulders will determine the movement and removal of sediments.

The state of the tide will mediate the degree of impact on macroalgae. If smothering occurs at low tide when the algae is lying flat on the substratum, then most of the organism as well as the associated community will be covered by the deposition of fine material at the level of the benchmark. Smothering will prevent photosynthesis resulting in reduced growth and eventually death. If, however, smothering occurs whilst the alga is submerged standing upright then the photosynthetic surfaces of adult plants could be left uncovered. The resistance of this biotope to the given pressure may vary with time of day. Germlings, however, are likely to be smothered and killed in both scenarios and are inherently most susceptible to this pressure. Indeed early life stages are smaller in size than adults and are thus most vulnerable to this pressure as even a small load of added sediment will lead to the complete burial. In general, propagules, early post-settlement stages and juveniles suffer severe stress and mortality from sediments (Devinny & Volse, 1978; Eriksson & Johansson, 2003; Berger et al., 2003; Vadas et al., 1992; Airoldi, 2003). Moss et al. (1973), for example, found that growth of zygotes of Himanthalia elongata were inhibited by a layer of silt 1-2 mm thick and that attachment on silt was insecure.

Increased abundance of algal turfs worldwide has been linked to sediment perturbations although not all the pathways and mechanisms of these effects are clear (see review by Airoldi, 2003).  However, even the most tolerant of organisms would eventually suffer from inhibition and mortality following smothering although the thresholds for these effects have has not been identified (Airoldi, 2003). Corallina officinalis and others within the genus (e.g. Corallina pinnatifolia and Corallina vancouveriensis) are found on shores subject to high rates of sedimentation that are periodically disturbed by sand burial and scour (Stewart, 1989).  Coralline turfs also trap sediments within the turf. The amount of sediment present and the associated fauna varies naturally depending on local conditions such as wave exposure (Dommasnes, 1969). On intertidal shores in southern California the amount of sediment trapped within turfs of Corallina spp. varied seasonally from <5 mm to >4.5 cm and was closely related to species composition and the structure of the turf. Airoldi (2003) identified a number of morphological, physiological and life history traits that conferred high levels of tolerance to sedimentation. Those shared by Corallina spp. are the regeneration of upright fronds from a perennial basal crust resistant to burial and scour, calcified thalli, apical meristems, large reproductive ouptuts, lateral vegetative growth and slow growth rates (Airoldi, 2003). Experimental deposition of sand on coralline turfs and maintained at 3 cm or 6 cm for one month via daily top-ups did not remove the turfs but did lead to rapid (within 1 hours) changes in the invertebrate species as highly mobile species moved away from the turf with later colonization by sand adapted species (Huff & Jarett, 2007). The community had recovered one month after sand deposition ceased (Huff & Jarett, 2007).

In a review of the effects of sedimentation on rocky coast assemblages, Airoldi (2003) outlined the evidence for the sensitivity of coralline algae to sedimentation. The reported results are contradictory with some authors suggesting that coralline algae are negatively affected by sediments while others report that encrusting corallines are often abundant or even dominant in a variety of sediment impacted habitats (Airoldi, 2003 and references therein). Crustose corallines have been reported to survive under a turf of filamentous algae and sediment for 58 days (the duration of experiment) in the Galapagos (species not identified, Kendrick, 1991). The crustose coralline Hydrolithon reinboldii has also been reported to survive deposition of silty sediments on subtidal reefs off Hawaii (Littler, 1973).

Atalah & Crowe (2010) added sediment to rockpools in controlled experiments that appear to be very similar to this biotope. The rockpools were occupied by a range of algae including encrusting corallines, turfs of Mastocarpus stellatus, Chondrus crispus and Corallina officinalis and green and red filamentous algae. The invertebrates present were mostly Patella ulyssiponensis, the winkle Littorina littorea and the flat topshell Gibbula umbilicalis. Sediment treatment involved the addition of a mixture of coarse and fine sand of either 300 mg/cm²/month or 600 mg/cm² every 15 days (the depth of sediment was not reported). The experimental treatments do not directly relate to the pressure benchmark but indicate some general trends in sensitivity. In the pools, the chronic addition of both levels of sediment led to a significant decrease in grazers and crustose coralline algae also decreased. Sedimentation had no significant effect on the cover of green filamentous algae (Ulva sp.) but led to an increase in the mean cover of red turfing algae (Mastocarpus stellatus and Chondrus crispus and Corallina officinalis) from 11.7% (±1.0 S.E.) in controls to 26.1% (±4.7 S.E.) in sedimented assemblages, but there were no differences between the two levels of sedimentation. The cover of red filamentous algae (Ceramium spp. and Gelidium spp.) was also significantly increased in the sedimentation experiments. The experimental results support the general trend of greater sensitivity of grazers and encrusting corallines to sedimentation than turf-forming algae.

Observations and experiments indicate that Ulva spp. have relatively high tolerances for the stresses induced by burial such as darkness, hypoxia and exposure to sulphides (Vermaat & Sand-Jensen, 1987; Corradi et al., 2006; Kamermans et al., 1998). Ulva lactuca is a dominant species on sand-affected rocky shores in New Hampshire (Daly & Mathieson, 1977), although Littler et al. (1983) suggest that Ulva sp. are present in areas periodically subject to sand deposition not because they are able to withstand burial but because they are able to rapidly colonize sand-scoured areas. Ulva spp. have, however, been reported to form turfs that trap sediments (Airoldi, 2003, references therein) suggesting that resistance to chronic rather than acute siltation events may be higher.

Sensitivity assessment. Deposition of 5 cm of fine material (see benchmark) in a single incident is unlikely to result in significant mortality before sediments are removed by current and wave action.  Burial will lower survival and germination rates of spores and cause some mortality in early life stages of Laminaria digitata and foliose red algae. Adults are more resistant but will experience a decrease in growth and photosynthetic rates.  Mortality will be reduced, and possibly avoided, where the smothering sediment is removed due to wave action or tidal streams, depending on how long the sediment remains.  Resistance has been assessed as ‘Medium’ as boulders are likely to project above the sediment surface and deposited sediments may be removed rapidly. Resilience is assessed as 'High'. Overall the biotope has a ‘Low’ sensitivity to smothering at the level of the benchmark.

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

Sensitivity to this pressure will be mediated by site-specific hydrodynamic conditions and the footprint of the impact. Where a large area is covered, sediments may be shifted by wave and tides rather than removed. However, mortality will depend on the duration of smothering, where wave action rapidly mobilizes and removes fine sediments, survival may be much greater. No evidence was found to assess this pressure at the benchmark. The degree to which boulders are smothered will depend on the size and shape. Where boulders are large they may project above the deposit although sediment re-suspension and scour during the tidal cycle will impact the epifauana and flora. A deposit at the pressure benchmark would cover sediments with a thick layer of fine materials and scour patterns around boulders will influence the time for the sediment to be removed.

Sensitivity assessment. At the level of the benchmark (30 cm of fine material added to the seabed in a single event) smothering is likely to result in mortalities of the Laminaria digitata understorey algae and invertebrates present on the boulders and within the sediments underlying the boulders. Resistance is assessed as ‘Low’ as many individuals exposed to siltation at the benchmark level are predicted to die and resilience is assessed as ‘Medium’. Overall the biotope is assessed as having ‘Medium’ sensitivity to siltation, at the pressure benchmark. 

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.

Underwater noise changes

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

Evidence

'Not relevant'.

Introduction of light or shading

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

Evidence

Increased levels of diffuse irradiation correlate with increased growth in macroalgae (Aguilera et al., 1999). Macroalgae require light to photosynthesize, so that changes in light intensity are likely to affect photosynthesis, growth, competition and survival. Chapman (1995) noted that too little or too much light are likely to be stressors. There is considerable literature on the light compensation point of marine algae (see Lüning, 1990) but it is difficult to correlate such evidence with 'shading', as light saturation and compensation points depend on light availability, light quality, season and turbidity. As Laminaria digitata is out-competed by Laminaria hyperborea in deeper waters, it is likely that permanent shading would affect their growth and allow them to be out-competed by other, more shade tolerant species, within the affected area. 

Corallina officinalis and other red algae are shade tolerant, often occurring under a macroalgal canopy that reduces light penetration. In areas of higher light levels, the fronds and bases may be lighter in colour due to bleaching (Colhart & Johansen, 1973). Other red algae in the biotope are flexible with regard to light levels. Canopy removal experiments in a rocky subtidal habitat in Nova Scotia, Canada, by Schmidt & Scheibling (2007) did not find a shift in understorey macroalgal turfs (dominated by Corallina officinalis, Chondrus crispus and Mastocarpus stellatus) to more light-adapted species over 18 months. Coralline crusts and Corallina officinalis are shade tolerant algae, often occurring under a macralgal canopy that reduces light penetration. These species can acclimate to different levels of light intensity and quality and encrusting corallines can occur in deeper water than other algae where light penetration is limited. Samples of Lithophyllum impressum suspended from a raft and shaded (50-75% light reduction) continued to grow over two years (Dethier, 1994). 

Sensitivity assessment. As Laminaria digitata are  out-competed in sublittoral conditions, it is likely that permanent shading would affect their growth and allow them to be out-competed by other, more shade tolerant species, such as red algae within the affected area, therefore a biotope resistance of 'Low' is suggested, with low confidence. Resilience is assessed as 'High' so that sensitivity is 'Low'.  

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

No direct evidence was found to assess this pressure. The associated macroalgae (with the exception of Ulva spp.) have limited dispersal, barriers and changes in tidal excursion are not considered relevant to these species as dispersal is limited.

Death or injury by collision

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

Evidence

'Not relevant’ to seabed habitats. NB. Collision by grounding vessels is addressed under ‘surface abrasion’.

Visual disturbance

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

Evidence

'Not relevant'.

Genetic modification & translocation of indigenous species

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

Evidence

No information was found on current production of Mastocarpus stellatus, Chondrus crispus or other turf forming red seaweeds in the UK and it is understood that wild harvesting rather than cultivation is the method of production. No evidence was found for the effects of gene flow between cultivated species and wild populations. Palmaria palmata may be cultivated for use as biofilters and/or food. Experiments by Van der Meer (1987) found that the hybrids of Palmaria palmata crosses from Canada and Ireland had vigorous growth and normal morphology, however, the tetraspores had lower viability and those that germinated produced abnormal sporelings. It was concluded that populations from Ireland and Canada represent the same species that is in the process of splitting into sibling species. Populations around the UK express different haplotypes (Provan et al., 2005) indicating some genetic variation between populations. Although cultivation of different genotypes may lead to gene flow between wild and cultivated populations, the limited dispersal may reduce exposure. Some negative effects may arise from hybridization between very geographically separated populations but there is no evidence to suggest that gene flow between different UK haplotypes would lead to negative effects.

Sensitivity assessment.  The pressure is considered to be '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 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; Heiser 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 had become 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 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 and 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 resulted in an increase in 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 have 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. 

The Pacific oyster Magallana gigas is a significant potential INIS as its distribution and environmental tolerances are considered to overlap with this biotope and this reef-forming species can alter habitat structure. It is found from the mid-littoral to the upper subtidal and grows on hard substrata but also on other bivalves (e.g., blue mussels) and polychaete reefs (Padilla, 2010). Diederich (2005, 2006) examined the settlement, recruitment and growth of Magallana gigas (as Crassostrea gigas) in the northern Wadden Sea. Recruitment of Magallana gigas was significantly higher in the intertidal than the shallow subtidal and the survival of adult oysters in the subtidal was limited by predation. Magallana gigas prefer to settle on conspecifics so it can build massive oyster reefs.   

The non-native crab Hemigrapsus sanguineus has recently been recorded in the UK (Sweet & Sewell, 2014) and has the potential to be a significant predator of intertidal invertebrates. Significant reductions in common shore crab abundance and mussel density have been reported where the crab has achieved high densities in mainland Europe (Sweet & Sewell, 2014). In Rye, New York, declines of approximately 80% of Littorina littorea in the intertidal were reported to coincide with an expansion of the Hemigrapsus sanguineus population (Kraemer et al., 2007). This crab occurs on exposed shores and may therefore occur in this biotope when established. If predation of littorinids was significantly increased this could impact the algal composition and abundance of this biotope by altering the level of grazing pressure. 

The carpet sea squirt Didemnum vexillum (syn. Didemnum vestitum; Didemnum vestum) is a colonial ascidian with rapidly expanding populations that have invaded most temperate coastal regions around the world (Kleeman, 2009; Stefaniak et al., 2012; Tillin et al., 2020). It is an ‘ecosystem engineer’ that can change or modify invaded habitats and alter biodiversity (Griffith et al., 2009; Mercer et al., 2009). Didemnum vexillum has colonized and established populations in the northeast Pacific, Canadian and USA coast; New Zealand; France, Spain, and the Wadden Sea, Netherlands; the Mediterranean Sea and Adriatic Sea (Bullard et al., 2007; Coutts & Forrest, 2007; Dijkstra et al., 2007; Valentine et al., 2007a; Valentine et al., 2007b; Lambert, 2009; Hitchin, 2012; Tagliapietra et al., 2012; Gittenberger et al., 2015; Vercaemer et al., 2015; Mckenzie et al., 2017; Cinar & Ozgul, 2023; Holt, 2024). In the UK, Didemnum vexillum has colonized Holyhead marina and Milford Haven, Wales; the west coast of Scotland (marinas around Largs, Clyde, Loch Creran and Loch Fyne), South Devon (Plymouth, Yealm, and Dartmouth estuaries), the Solent, northern Kent, Essex, and Suffolk coasts (Griffith et al., 2009; Lambert, 2009; Hitchin, 2012; Michin & Nunn, 2013; Bishop et al., 2015; Mckenzie et al., 2017; Tillin et al., 2020, Holt, 2024; NBN, 2024).

Although a widespread invader, Didemnum vexillum has a limited ability for natural dispersal since the pelagic larvae remain in the water column for a short time (up to 36 hours). Therefore, it has a short dispersal phase that can allow the species to build localized populations (Herborg et al., 2009; Vercaemer et al., 2015; Holt, 2024). However, Bullard et al. (2007) suggested that Didemnum vexillum can form new colonies asexually by fragmentation. Colonies can produce long tendrils from an encrusting colony, which can fragment, disperse and settle, attaching to suitable hard substrata elsewhere (Bullard et al., 2007; Lambert, 2009; Stefaniak & Whitlatch, 2014). A fragmented colony can spread naturally for up to three weeks transported by ocean currents, attached to floating seaweed, seagrass or other floating biota, or as free-floating spherical colonies (Bullard et al., 2007; Lengyel et al., 2009; Stefaniak & Whitlatch, 2014; Holt, 2024). Fragments can reattach to suitable substrata within six hours of contact. Fragments have the potential to disperse around 20 km before reattachment (Lengyel et al., 2009). Valentine et al. (2007a) reported that colonies of Didemnum vexillum enlarged by 6 to 11 times by asexual budding after 15 days and enlarged 11 to 19 times after 30 days. Valentine et al. (2007a) concluded fragments could successfully grow, survive, and help to spread Didemnum vexillum.

While natural fragmentation of tendrils is thought to allow Didemnum vexillum to invade longer distances and increase its dispersal potential, Stefaniak & Whitlatch (2014) found that only one tendril out of 80 reattached to the flat, bare substrata used in their study, because tendrils required an extensive (at least eight hour) period of contact to reattach. Stefaniak & Whitlatch (2014) suggested that once fragmented from a colony, the success of tendril reattachment was limited, and reattachment was not a major contributor to the invasive success of Didemnum vexillum. However, Stefaniak & Whitlatch (2014) also found that larvae-packed tendril fragments may increase natural dispersal distance, reproduction, and invasive success of Didemnum vexillum, and increase the distance larvae can travel. Not all colonies produce tendrils at all locations.

Human-meditated transport via aquaculture facilities, boat hulls, commercial fishing vessels, and ballast water is probably the most important vector that has aided the long-distance dispersal of Didemnum vexillum and explains its prevalence in harbours and marinas (Bullard et al., 2007; Dijkstra et al., 2007; Griffith et al., 2009; Herborg et al., 2009). Fragmentation of colonies during transport or human disturbance (such as trawling or dredging) could indirectly disperse the species and enable it to find suitable conditions for establishment (Herborg et al., 2009). For example, in oyster farms in British Columbia, large fragments of Didemnum sp. come off oyster strings when they are pulled out of water and other fragments can be pulled off oysters and mussels and thrown back into the water, which is likely to aid dispersal of the invasive species (Bullard et al., 2007). Dijkstra et al. (2007) hypothesised that Didemnum sp. was introduced to the Gulf of Maine with oyster aquaculture in the Damariscotta River and transported via Pacific oysters.

Didemnum vexillum was likely introduced into the UK from northern Europe or Ireland via poorly maintained or not antifouled vessels, movement of contaminated shellfish stock and aquaculture equipment, or via marine industries such as oil, gas, renewables, and dredging (Holt, 2024). Recent evidence from genetic material suggests that human-mediated dispersal, between marinas and shellfish culture sites, is the most likely pathway for connectivity of Didemnum vexillum populations throughout Ireland and Britain (Prentice et al., 2021; Holt, 2024). Didemnum vexillum can disperse away from artificial substrata, invading and colonizing natural substrata in surrounding areas (Tillin et al., 2020). Holt (2024) noted that Didemnum vexillum had not spread as far as feared in the UK since it was first recorded. The current evidence of Didemnum vexillum’s ability to spread on natural habitats in this area is sparse and often conflicting, complicated by genetics and its apparent variable habitat preferences and tolerances and its variable ability to adapt to ‘new’ conditions (Holt 2024).

Didemnum vexillum has a seasonal growth cycle influenced by temperature (Valentine et al., 2007a). In warmer months (June and July) colonies may be large and well-developed encrusting mats. Populations experience more rapid growth from July to September sometimes continuing into December. Colonies begin to decline in health and ‘die-off’ when temperatures drop below 5°C during winter months from around October to April (Gittenberger, 2007; Valentine et al., 2007a; Herborg et al., 2009). Cold water months cause colonies to regress and reduce in size, yet they often regenerate as temperatures warm (Griffith et al., 2009; Kleeman, 2009, Mercer et al., 2009), although some populations may not survive winter at all (Dijkstra et al., 2007). The early growth phase, from May to July, is initiated by smaller colonies developing from remnants of colonies that survived the cold water (Valentine et al., 2007a). The seasonal growth cycle is also likely influenced by location. For example, the Didemnum sp. growth cycle for colonies in Sandwich tide pool (temperature range from -1 °C to 24 °C, with daily fluctuations), probably does not occur in deep offshore subtidal habitats in Georges Bank (annual temperature range from 4 °C to 15°C, and daily fluctuations are minimal) (Valentine et al., 2007a).  Larval release and recruitment typically occur between 14 to 20°C and slow or cease below 9 to 11°C as summer ends (Griffith et al., 2009; Mckenzie et al., 2017). In New Zealand, recruitment occurs from November to July, where the highest average temperatures were recorded in February (18 to 22°C) and the lowest average temperatures were recorded in July (9 to 10°C) (Fletcher et al., 2013a). In this New Zealand study, higher water temperatures were associated with a higher level of recruitment (Fletcher et al., 2013a).

Didemnum vexillum requires suitable hard substrata for successful settlement and the establishment of colonies. It can grow quickly and establish large colonies of dense encrusting mats on a variety of hard substrata (Valentine et al., 2007a; Griffith et al., 2009; Lambert, 2009; Groner et al., 2011; Cinar & Ozgul, 2023). Gittenberger (2007) stated that invasive Didemnum sp. was a threat to native ecosystems because of its ability to overgrow virtually all hard substrata present. Suitable hard substrata can include rocky substrata such as bedrock gravel, pebble, cobble, or boulders or artificial substrata such as a variety of maritime structures such as pontoons, docks, wood and metal pilings, chains, ropes and moorings, plastic and ship hulls and at aquaculture facilities (Valentine et al., 2007 a&b; Bullard et al., 2007; Griffith et al., 2009; Lambert, 2009; Tagliapietra et al., 2012; Tillin et al., 2020). Didemnum vexillum has been reported colonizing these types of hard substrata in the USA, Canada, northern Kent, and the Solent (Bullard et al., 2007; Valentine et al., 2007a; Valentine et al., 2007b; Hitchin, 2012; Vercaemer et al., 2015; Tillin et al., 2020).

Didemnum sp. can colonize both horizontal and vertical surfaces of fouling and benthic communities, commonly occurring on upper horizontal surfaces in benthic habitats (Dijkstra et al., 2007; Tillin et al., 2020). It has been recorded on overhangs or the underside of boulders (Hitchin, 2012) or the underside of docks, boat hulls, and pontoons (Griffiths et al., 2009; Minchin & Nunn, 2013). In sheltered areas, colonies are lobed and beard-like, forming long tendrils that drop down from the underside of docks or other artificial substrata to establish new colonies if there is suitable substrata available (Valentine et al., 2007a). In areas of stronger current, colonies are low undulating mats (Valentine et al., 2007 a&b).

Didemnum vexillum has the ability to rapidly overgrow and displace on other sessile organisms such as other colonial ascidians (Ciona intestinalis, Styela clava, Ascidiella aspera, Botrylloides violaceus, Botryllus schlosseri, Diplosoma listerianium and Aplidium spp.), bryozoan, hydroids, sponges (Clione celata and Halichrondria sp.), anemone (Diadumene cincta), calcareous tube worms, eelgrass (Zostera marina), kelp (Laminaria spp. and Agarum sp.), green algae (Codium fragile subsp. fragile), red algae (Plocamium, Chondrus crispus and bush weed Agardhiella subulata), brown algae (Ascophyllum nodosum, Sargassum, Halidrys, Fucus evanescens and Fucus serratus), calcareous algae (Corallina officinalis), mussels (Mytilus galloprovincialis, Perna canaliculus  and Mytilus edulis), barnacles, oysters (Magallana gigas, Ostrea edulis and Crassostrea virginica), sea scallops (Placopecten magellanicus), or dead shells (Dijkstra et al., 2007; Gittenberger, 2007; Valentine et al., 2007a; Valentine et al., 2007b; Griffith et al., 2009; Carman & Grunden, 2010; Dijkstra & Nolan, 2011; Groner et al., 2011; Hitchin, 2012; Tagliapietra et al., 2012; Minchin & Nunn, 2013; Gittenberger et al., 2015; Long & Groholz, 2015; Vercaemer et al., 2015).

Some species have been shown to tolerate overgrowth by Didemnum vexillum. Such as anemones (did not specify species name) that were observed in high densities of 10 to 339 individuals in transects with a high percentage cover of Didemnum vexillum (Lengyel et al., 2009). In the Netherlands, the sea anemone Sagartia elegans and Sabella pavonia tubes were not overgrown by Didemnum sp. (Gittenberger, 2007). Botrylloides violaceus can overgrow Didemnum sp. (Gittenberger, 2007) although it was noted to be overgrown in other studies (Valentine et al., 2007a). In addition, Styela clava and Ascidiella aspera survived overgrowth by Didemnum vexillum as long as their siphons remained free (Gittenberger, 2007). However, Gittenberger (2007) stated that the boring sponge Clione celata, the sea anemone Diadumene cincta, Mytilus edulis, Magallana (syn. Crassostrea) gigas, Ostrea edulis, a variety of hydroids, the colonial ascidians Aplidium (Fig. 4) and Diplosoma listerianum and the solitary ascidians Ciona intestinalis start to die on contact with Didemnum sp.

In contrast to Didemnum vexillum’s preference for sheltered conditions, established colonies observed in Georges Bank and Long Island Sound were exposed to moderately strong tidal currents (1 to 2 knots; ca 0.5 to 1 m/s recorded at both sites) that may mobilise sediment (Valentine et al., 2007b; Mercer et al., 2009; Tillin et al., 2020). However, Valentine et al. (2007b) describe the substratum as immobile, presumably consolidated gravel, cobbles and pebbles. Kleeman (2009), stated that the presence of a consistent mild wave action or ‘swash zone’ appears to favour Didemnum sp. establishment in the intertidal. Although some evidence suggests that waves and currents can facilitate the fragmentation and spread of Didemnum vexillum (Mckenzie et al., 2017), the tidal current velocities at some sites where Didemnum vexillum has been reported (for example, New England, where current velocities reach up to around 3 m/s) is lower than the current velocity required for the dislodgement of Didemnum vexillum fragments (around 7.6 m/s) (Reinhardt et al., 2012). This suggests that not all tidal currents are likely to dislodge Didemnum vexillum fragments. When on boat hulls the species can experience higher current velocities which is enough to cause dislodgement (Reinhardt et al., 2012).  

Sensitivity Assessment. The above evidence suggests that Undaria pinnatifida can co-exist with native kelp species within its depth range (-1 to 4 m) e.g., Laminaria digitata as shown in Plymouth Sound, UK. The dense kelp canopy may restrict or slow the proliferation of Undaria pinnatifida. But Laminaria digitata has been shown to out-compete Undaria pinnatifida. For example, removal of the Laminaria digitata canopy resulted in the increase of Undaria pinnatifida abundance but recovery of Laminaria digitata in the following year resulted in a concurrent decline in Undaria pinnatifida. 

In addition, this Laminaria digitata dominated biotope (IR.MIR.KR.Ldig.Bo) is found in the sublittoral fringe with a wave exposure ranging from moderately exposed to sheltered and is structured by moderately strong to very weak tidal streams. The evidence above suggests that Undaria prefers sheltered conditions, with low tidal flow, and is less tolerant of desiccation than Laminaria digitata.  It is unlikely to out-compete or replace Laminaria digitata under the physical conditions that characterize this biotope. Therefore, resistance is assessed as ‘Medium’ to represent the possibility of short-term colonization by Undaria after a disturbance. Resilience is ‘High’ due to the high fitness nature of Laminaria digitata (Epstein et al., 2019b), so sensitivity is assessed as ‘Low’.  

However, while Sargassum muticum prefers wave-sheltered, shallow sites in the sublittoral fringe, it has been reported to invade and out-compete Laminaria digitata beds in Normandy, France (Cosson, 1999; de Bettignies et al., 2021).  Therefore, resistance is assessed as ‘Low’ to represent the possibility of colonization by Sargassum.  While Laminaria digitata may out-compete Undaria, the recovery after invasion by Sargassum, although rapid, would require direct intervention (removal). Hence, resilience is probably ‘Very low’ so sensitivity is assessed as ‘High’. Overall, confidence is assessed as ‘Low’ due to evidence of variation and the site-specific nature of competition between native kelps and both Undaria pinnatifida and Sargassum muticum and the limited direct evidence of the effect of Sargassum on Laminaria digitata. 

There is no evidence of Didemnum vexillum colonizing this biotope in the UK. Didemnum vexillum requires hard substrata for successful colonization and has been recorded colonizing sides of boulders (Hitchen, 2012). therefore, it could colonize the boulders that characterize this biotope. Didemnum vexillum can overgrow and displace sessile organisms, including brown algae species Ascophyllum nodosum, Sargassum, Fucus evanescens and Fucus serratus (Gittenberger, 2007; Valentine et al., 2007a). However, there is no evidence on how Didemnum vexillum affects fucoids or if it causes fucoid mortality.  In more wave-exposed examples of this biotope, where boulders are more mobile the abundance of Didemnum vexillum will be limited but sheltered examples may be more vulnerable. Under-boulder communities are determined by competition for space and Didemnum vexillum is likely to compete with other ascidians, bryozoans and encrusting epifauna, which could potentially interfere with their recruitment, and lead to mortality and a reduction in biodiversity.  Therefore, a resistance of 'Low' is suggested as a precaution but with 'Low' confidence due to the lack of direct evidence. Resilience is likely to be 'Very low' as Didemnum vexillum would need to be physically removed to allow recovery. Hence, sensitivity to invasion by Didemnum is assessed as 'High'. 

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

Symptoms of disease are regularly seen on Laminaria species, however, little evidence in the literature is apparent. Infection of Laminaria japonica sporophytes by Pseudoalteromonas, Vibrio and Halomonas results in the characteristic symptoms of hole-rotten disease (Wang et al., 2008). Additionally, red spot disease may be caused by bacteria of the genus Alteromonas (Sawabe et al., 1998). Hyperplasia or gall growths are often seen as dark spots on Laminaria digitata and have been associated with endophytic brown filamentous algae. It can be inferred from these observations that microbial pathogens may impact growth rates of individuals. There is no evidence in the literature that infection by microbial pathogens results in mass death of Laminaria populations and the kelp themselves are known to regulate bacterial infections through iodine metabolism (Cosse et al., 2009).

Several coralline and non-coralline species are epiphytic on Corallina officinalis. Irvine & Chamberlain (1994) cite tissue destruction caused by Titanoderma corallinae. However, no information on pathogenic organisms in the UK was found. Corallina officinalis, like many other algal species has been demonstrated to produce antibacterial substances (Taskin et al., 2007). No evidence was found for pathogens of the other red algae which may be present in this biotope. The fungal pathogen, Petersenia palmaria n. sp (Oomycetes) which infects Palmaria mollis, does not affect Palmaria palmata (Meer & Pueschel, 1985).

Other species associated with this biotope may experience low levels of infestation by pathogens but mass-mortalities have not been recorded. Barnacles are parasitized by a variety of organisms and, in particular, the cryptoniscid isopod Hemioniscus balani, in which heavy infestation can cause castration of the barnacle.  At usual levels of infestation these are not considered to lead to high levels of mortality.  

Diseased encrusting corallines were first observed in the tropics in the early 1990’s when the bacterial pathogen Coralline Lethal Orange Disease (CLOD) was discovered (Littler & Littler, 1995). All species of articulated and crustose species tested to date are easily infected by CLOD and it has been increasing in occurrence at sites where first observed and spreading through the tropics. Another bacterial pathogen causing a similar CLOD disease has been observed with a greater distribution and a black fungal pathogen first discovered in American Samoa has been dispersing (Littler & Littler, 1998). An unknown pathogen has also been reported to lead to white ‘target-shaped’ marks on corallines, again in the tropic (Littler et al., 2007). No evidence was found that these are impacting temperate coralline habitats.

Sensitivity assessment. No evidence was found that outbreaks of microbial pathogens significantly impact populations of the key characterizing Laminaria digitata and other associated algal species.  Biotope resistance is, therefore, assessed as ‘High’ and resilience as ‘High’, so that the biotope is considered to be ‘Not sensitive’. 

Removal of target species

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

Evidence

Direct, physical impacts from harvesting are assessed through the abrasion and penetration of the seabed pressures. The sensitivity assessment for this pressure considers any biological/ecological effects resulting from the removal of target species on this biotope. Many of the algal species characterizing or associated with this biotope may be targeted by either recreational or commercial harvesters.

Traditionally Laminaria digitata was added to agricultural lands as fertilizers; now Laminaria species are used in a range of different products, with its alginates used in the cosmetic, pharmaceutical and agri-food industries (Kervarec et al., 1999; McHugh, 2003). In France, Laminaria digitata is harvested with a ‘Scoubidou’ (a curved iron hook which is mechanically operated). This device is considered to be selective; only harvesting individuals older than 2 years (Arzel, 2002). France reportedly harvests 75,000t kelp, mainly consisting of Laminaria digitata annually (FAO, 2007). Davoult et al. (2011) suggested that the maintenance of a sustainable crop of Laminaria digitata was possible if the industry continues employing small vessels evenly dispersed along the coastline. This would protect against habitat fragmentation and buffer over exploitation (Davoult et al., 2011). A fallow period of 18-24 months has been suggested for Laminaria digitata in France, where competition between the juvenile sporophytes of Laminaria digitata and Saccorhiza polyschides was indicated as a threat to the continued harvesting effort of Laminaria digitata (Engelen et al., 2011). If Laminaria digitata, the key characterizing and structuring species of this biotope is removed then the biotope, is considered lost due to the significant alteration to the biotope classification and character of the habitat is likely.

Canopy removal of Laminaria digitata has been shown to reduce shading, resulting in the bleaching of sub-canopy algae (Hawkins & Harkin, 1985). Harvesting may also result in habitat fragmentation, a major threat to this biotope’s ecosystem functioning (Valero et al., 2011). In the UK, harvesting of Laminaria digitata is currently restricted to manual removal and farming on small scales.

Red algae within the biotope may also be subject to hand gathering. Mastocarpus stellatus is harvested commercially in Scotland and Ireland to produce carrageen, the stipe is removed but the base is left intact to allow the algae to re-grow. Palmaria palmata and Osmundea pinnatifida are also collected by hand commercially and recreationally for consumption. Corallina officinalis is collected for medical purposes; the fronds are dried and converted to hydroxyapatite and used as bone forming material (Ewers et al., 1987). It is also sold as a powder for use in the cosmetic industry.

Sensitivity assessment. As the macroalgae species that are harvested in this biotope are attached and conspicuous, a single event of targeted harvesting could efficiently remove individuals and resistance is assessed as ‘Low’. Resilience of Laminaria digitata and the turf forming red seaweeds is assessed as ‘High’ (based on evidence for recovery from harvesting that did not damage the algal bases, although see caveats in the resilience section) and biotope sensitivity is assessed as ‘Low'. This assessment refers to a single collection event, long-term harvesting over wide spatial scales will lead to greater impacts, with lower resistance and longer recovery times.

Removal of non-target species

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

Evidence

Direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures, while this pressure considers the ecological or biological effects of incidental removal of species. Removal of a large proportion of the brown and red macroalgae would substantially alter the character of the biotope. Loss of the characterizing and associated species would also alter ecosystem functions, such as rates of production and the provision of a structurally complex habitat.

Sensitivity assessment. Removal of species as by-catch would remove the biological assemblage that defines the biotope, hence the biotope is considered to have ‘Low’ resistance to this pressure and to have ‘Medium’ resilience. Biotope sensitivity is therefore ‘Medium’.