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

Saccharina latissima is found in the NW Atlantic and North Pacific (Wilce 1965;  Druehl, 1970; Lüning, 1990), typically occurring between 40°N and 80°N. In Europe, Saccharina latissima occurs from Portugal to Spitbergen (Van den Hoek & Donze, 1967, Lüning, 1990).  Its distribution suggests a tolerance to a chronic temperature change (e.g. by 2°C for a year).  Other associated organisms to this biotope may fair less well.  Exposure to high short-term temperature increases are likely to result in stress, however the recovery of this biotope is likely to be rapid.  There is a general consensus in the literature that increases in temperature are likely to have a more detrimental effect than decreases in temperature (Andersen et al., 2013, Nielsen et al., 2014).

Temperature ecotypes have been suggested for Saccharina latissima populations near its southern limit off the USA coastline. Algae from New York, which experience water temperatures in excess of 20°C each summer, exhibit greater temperature tolerance than algae from Maine, where temperatures rarely exceed 17°C (Gerard & Du Bois, 1988). Three weeks of exposure to temperatures greater than 20°C in the field resulted in 50% mortality of algae from New York, while 100% of the algae from Maine died (Gerard & Du Bois, 1988). In comparison, individual  Saccharina latissima from Helgoland in the southern North Sea undergo disintegration of blade tissue after 3 month at 15°C (Lüning, 1988).

The life cycle of kelps are considered sensitive to temperature. At temperatures greater than 15°C, higher photon flux densities are required to reach similar proportions of fertility to their counterparts kept at lower temperatures (Lüning, 1990), while photon fluence rates have been noted to rise concomitantly whilst photosynthetic efficiency decreases (Davison et al., 1991). Sporogenesis in Saccharina latissima requires a minimum period of 4 weeks at or below 15°C combined with short day lengths in order to occur (Müller et al., 2009).  Germination of zoospores is also sensitive to temperature and may be population specific, with germination inhibited at 20°C in the laboratory, but exceeding 90% in field populations collected in July when photo fluence rates were 5 µE m^-2 sec^-1 (Lee & Brinkhuis, 1988). The same study found that gametophyte growth improved with increasing water temperatures between 4-17°C and that fecundity was greatest between 7-17°C.

Sporophyte growth has been recorded between 10-15°C with 50-70% reduction in growth at 20°C (Bolton & Lüning, 1982). For the gametophytes and young sporophytes of Saccharina latissima, the upper temperature tolerance is 22°C with exceptions including the growth of gametophytes in Long Island Sound at 23°C (Lee & Brinkhuis, 1988). A temperature of 23°C is also considered to be the maximum survival temperature for gametophytes from three European populations of Saccharina latissima, with disintegration occurring after 3 weeks (Bolton & Lüning, 1982). Although a more conservative estimate of Saccharina latissima’s upper temperature limit was considered by Lüning (1990) to be 20°C. In the summer of 1983 (the hottest on record before July 2009), bleaching of Saccharina latissima sporophytes was evident in Plymouth Sound and on the Isle of Man (Hawkins & Hartnoll, 1985). Research showed that growth reduction was evident at only 5°C above the optimum temperature range for Saccharina latissima (10-15°C) (Kain 1979; Bolton & Lüning 1982; Andersen et al., 2013).

In an experiment observing gene expression in Saccharina latissima, a greater representation of genes associated with high temperature response than those for low temperatures was evident, suggesting that higher temperatures are more detrimental to Saccharina latissima (and therefore the biotope) than low temperatures (Heinrich et al., 2012). A permanent change to the local temperature regime may result in a shift to ephemeral algae which then form a barrier to future settlement of Saccharina latissima slowing or stopping recovery of the biotope (Moy & Christie, 2012).

Laminaria digitata is distributed from Brittany to the Spitzbergen (Birkett et al., 1998b; Blight & Thompson, 2008). The Northern/Boreal distribution of Laminaria digitata suggests it may be slightly vulnerable to temperature increases in its southern range. The thermal optimum of Laminaria digitata is between 10-15°C, with reproductive ability impaired to 20% at 18°C (Arzel, 1998). 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. A temperature increase to 22-23 °C causes cell damage and death (Sudene, 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 and recruitment (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 it’s northern limits and localised extinctions across it’s 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 summer sea temperature (Bartsch et al. 2013). In southern examples of the biotope, Laminaria digitata may also be out-competed by it’s Lusitanian competitor Laminaria ochroleuca which is regionally abundant across the south UK coastline (Smale et al., 2014).

Increased temperatures bring with them increased growth of epiphytic ephemeral algae. Excessive growth on kelp by these species has been reported to result in high mortality rates within the kelp populations on the North American coast (Lee & Brinkhuis, 1988, Levin et al., 2002, Scheibling & Gagnon, 2006).  Krumhansl & Scheibling (2011) also found negative effects in growth in conjunction with increasing temperatures, however they also highlighted the role which ephiphytic loading enhances blade tissue loss (Andersen et al., 2013).  If environmental conditions for spore survival are not favourable, then development of the gametophytes can be delayed for a short period, creating a level of resistance against short-term environmental changes (Van den Hoek et al., 1995). Despite this ability, seaweeds in general are considered particularly vulnerable to short-term warming events (Dayton & Tegner, 1984; Smale & Wernberg, 2013; Wernberg et al., 2013; from Smale et al., 2013). Recruitment of Saccharina latissima generally occurs in the highest numbers from December to January (Andersen et al., 2011).

The tolerance of red algae to temperature changes varies considerably and those of the littoral zone typically have a greater tolerance to both increased and decreased temperature, than those of the sublittoral (see Gessner, 1970). Sublittoral red algal species, Sphondylothamnion multifidum, Cryptopleura ramosa and Rhodophyllis divaricata were capable of surviving at 27 °C, while other species such as Callophyllis laciniata, Calliblepharis ciliata, Plocamium cartilagineum and Heterosiphonia plumosa died within 12 hours in seawater at 27 °C. However, such a temperature increase exceeds that of the benchmark level. There is some evidence to suggest that blade growth in Delesseria sanguinea is delayed until ambient sea temperatures fall below 13°C, although blade growth is likely to be intrinsically linked to gametangia development (see Kain, 1987). Delesseria sanguinea is tolerant of 23°C for a week (Lüning, 1984) but dies rapidly at 25°C. North Sea and Baltic specimens grew between 0-20°C, survived at 23°C but died at 25°C rapidly (Rietema, 1993). Rietema (1993) reported temperature differences in temperature tolerance between North Sea and Baltic specimens. Lüning (1990) reports optimal growth in Delesseria sanguinea between 10 -15°C and optimal photosynthesis at 20°C. However, the upper limit of temperature tolerance is reduced by lowered salinity in Baltic specimens (Kinne, 1970; Kain & Norton, 1990). At low salinity photosynthesis is restricted to a narrow range of temperatures in adult thalli whereas juvenile thalli have a wider response range (Lobban & Harrison, 1997; fig 6.27). It is likely therefore that within the subtidal an increase in temperature of 2°C in the long-term will have limited effect on survival, although it may affect initiation of new growth at the southern limits of the population. An increase of 5°C in the short-term may affect survival if the ambient temperature is increased above 23°C.

Sensitivity assessment. Responses of this biotope to an increase in temperature are clearly population specific. Those at the extremes of the biotope’s temperature range are likely to be more affected than those at the centre of their range. An increase of 5°C for one month may affect the fecundity of Saccharina latissima or Laminaria digitata for that year depending on when the increase occurs. An increase of 2°C is more likely to affect those at the extremes of the biotope’s range, the plasticity of Saccharina latissima may allow for populations to adapt to the new conditions over time, however this is uncertain. Similarly, Laminaria digitata may survive a short-term increase in temperature (5°C for one month) but a long-term increase (2°C for one year) may result in loss of a proportion of the population especially at its upper extent on the shore and/or in southern parts of its range in summer months.  The red algae community may survive long-term increase in 2°C but may suffer mortality from short-term change by 5°C, especially if the resultant temperature exceeded 27°C. Therefore resistance of this biotope to an increase in temperature is therefore considered as ‘Medium’ at the benchmark level. Resilience is likely to be ‘High’ and sensitivity therefore ‘Low’. However, prolonged increases in temperature or espacially hot summers (see Sundene, 1964)  may result in loss of Laminaria digitata from the biotope, and hence a loss of the biotope.

Temperature decrease (local)

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

Evidence

Saccharina latissima is found in the NW Atlantic and North Pacific (Wilce 1965;  Druehl, 1970; Lüning 1990), typically occurring between 40°N and 80°N. In Europe, Saccharina latissima occurs from Portugal to Spitbergen (Van den Hoek & Donze, 1967, Lüning, 1990). Its distribution suggest that the species would tolerate a chronic temperature change (e.g. by 2°C for a year).  Laminaria digitata is distributed from Brittany to the Spitzbergen (Birkett et al., 1998; Blight & Thompson, 2008). The Northern/Boreal distribution of Laminaria digitata suggests it would tolerate a decrease in temperature at the benchmark level.

The life cycle of kelps, in particular their spore production stage is considered to be sensitive to temperature.  The gametophytes of Saccharina latissima reportedly suppress growth below 10°C (Lüning, 1990). In a laboratory experiment with an Arctic population of Saccharina latissima, embryos achieved 100% germination at 0°C, but expressed lower rates of primary cell growth in comparison to those grown at 10°C. These lower rates of growth do not seem to impede the kelp’s ability to compete successfully, with the species occurring in year round temperatures lower than 0°C in a high-arctic Fjord, Greenland (Borum et al., 2002). Sjotun & Schoschina (2002) cultivated Saccharina latissima from embryospores at 0°C in the laboratory and showed that oogonia were produced 18-20 days after sporulation in comparison to a minimum of 20-24 days for Laminaria hyperborea, and 34 days for Laminaria digitata.

Under laboratory conditions chronic exposure to 5°C, after being maintained at 15°C, resulted in the adult sporophytes stage requiring a higher photon fluence rate to maintain net and light-saturated photosynthesis (studied as Laminaria saccharina, Davison et al., 1991). This response is short-term, with the acclimation of growth temperatures over time buffering the depression in compensation point and light-saturated photosynthesis, allowing the alga to achieve similar rates of light-limited photosynthesis at both 5 and 15°C (Davison et al., 1991). At 2°C, Saccharina latissima up-regulates the production of amino acids associated with Glutathione, an antioxidant, suggesting that below 2°C lowered growth rates are related to an increased energy expenditure on decreasing the effects of photo-oxidative stress (Heinrich et al., 2012). 

The thermal optimum of Laminaria digitata is between 10-15°C, with reproductive ability impaired to 20% at 18°C (Arzel, 1998). 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. A temperature increase to 22-23°C causes cell damage and death (Sudene, 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, 2013). A minimum of 10 weeks a year between 5-18 °C is needed in order to ensure spore formation and hence reproduction and recruitment (Bartsch, 2013).

Cold damage usually changes the colour of red algae to a bright yellow orange. Sphondylothamnion multifidum, Cryptopleura ramosa and Rhodophyllis divaricata were partially or completely killed at 5°C. Callophyllis laciniata, Calliblepharis ciliata, Plocamium cartilagineum and Heterosiphonia plumosa survived -2°C. Delesseria sanguinea and Phycodrys rubens succumbed at temperatures of -3°C to -5°C. During experimental attempts to adapt red algae to cold by maintaining them at -1°C to + 1°C for several months, a drop in the lethal temperature tolerance of Delesseria sanguinea and a few other species was detected, in the order of 1 to 2°C (Gessner, 1970). However, it is unlikely that seawater temperatures would fall below 0°C in the UK.

Sensitivity assessment. A decrease in temperature at the benchmark is not likely to impact biotopes at the centre of their temperature tolerances, however those at its temperature limit are likely to experience decreases in abundance of Saccharina latissima  (due to reduced reproduction and growth) if the temperature is lowered to 0°C for one year.  As Laminaria digitata is a northern boreal species, a chronic reduction in temrpature is unlkely to be significant.  If decreases of 5°C for one month occur, then the time of the year is vital in determining the response of this biotope as it may impact the fecundity of the Saccharina latissima population and growth of red algae. However, if the decrease is chronic the biotope should persist and is therefore considered to have a resistance of ‘High’ to this biotope. A resilience of ‘High’ is therefore also recorded, while the overall sensitivity of the biotope is ‘Not sensitive’, although beyond the benchmark, the loss of the biotope may occur.

Salinity increase (local)

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

Evidence

IR.LIR.K.Slat.Ldig is recorded from full or variable salinity conditions but Saccharina latissima is also typical of reduced salinity conditions (Connor et al., 2004).  In a laboratory experiment, Saccharina latissima (studied as Laminaria saccharina) survived successfully between 17-32 psu (Druehl, 1967). However, Gerard & Du Bois (1988) reported that Saccharina latissima had a salinity tolerance of 23-31 psu. Karsten (2007) tested the photosynthetic ability of Saccharina latissima under acute 2 and 5 day exposure to salinity treatments ranging from 5-60 psu. A control experiment was also carried at 34 psu. Saccharina latissima showed high photosynthetic ability at >80% of the control levels between 25-55 psu. Decreases in salinity to 5 psu for Saccharina latissima from Arctic Kongsfjorden (Spitsbergen) induced bleaching, indicative of cell damage after 5 days of incubation in the laboratory, while treatments decreasing from 20-10 psu were associated with decreasing photosynthetic performance (Karsten, 2007).  However, Birkett et al. (1998b) suggested that kelps are stenohaline and, therefore, long-term increases in salinity may be detrimental.

Optimum growth rates in Saccharina latissima cultured from UK waters were achieved at 31 psu, while 16 psu dramatically decreased growth rates and 8 psu resulted in the death of the alga (Burrows & Pybus 1971).  In contrast, Saccharina latissima from the White Sea responded with decreased photosynthetic rates at 6-8 psu, while severe growth reductions were noted at 2 psu (Drobyshev, 1971).  Juvenile sporophytes of Saccharina latissima can survive salinities of 13 for 3 weeks however, at 10 psu the juveniles become severely stressed and the majority die (Spurkland & Iken, 2011a).  In Arctic kelp, decreases in Saccharina latissima growth were associated with decreasing salinity (Spurkland & Iken 2011a).  Nielsen et al. (2014) also associated low growth, with decreases in salinity in a field experiment in Danish waters; while Weile (1996), recorded low growths (5.4 mm/day) in areas <14 psu. Responses of Saccharina latissima to salinity changes are population specific. Exposure to salinities outside a kelp’s tolerance range causes osmotic and ionic stress (Kirst 1990) resulting in decreased efficiency of their photosynthetic apparatus (<20-25%, Kirst & Wiencke, 1995).

At the extremes of Laminaria digitata’s salinity tolerance, decreases in photosynthetic rates are evident, particularly at low salinities (Gordillo et al., 2002).  On the Norwegian coast which is subjected to seasonal fluctuations in salinity, healthy Laminaria digitata plants were found growing at 15-25 psu (Sundene, 1964).  Long-term reductions in salinity may result in the loss of the kelp beds in the affected area, or the out-competition of Saccharina latissima by Laminaria digitata, and thus the loss of the biotope (Birkett et al., 1998b). Kelp tolerate increases in salinity better than decreases in salinity, with no evidence of decreased photosynthetic activity at 55 psu (Karsten, 2007). Laminaria digitata tolerates a large salinity range within a 24 hour period (5-60psu; Karsten, 2007).

Sensitivity assessment. At the benchmark, an increase in salinity from 'full' to 'hypersaline' (>40 psu) conditions for a year is unlikely to adversely affect Saccharina latissima or Laminaria digitata as kelp tolerate increases in salinity better than decreases in salinity, with no evidence of decreased photosynthetic activity at 55psu (Karsten, 2007).  Little evidence for the effects of hypersaline conditions on the associated flora and fauna was found. Therefore, the resistance is probably 'Medium' to represent the potential loss of members of the associated flora and fauna. Resilience ins probably 'High' so that sensitivity is assessed as 'Low'.

Salinity decrease (local)

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

Evidence

IR.LIR.K.Slat.Ldig is recorded from full or variable conditions but Saccharina latissima is also typical of reduced salinity conditions (Connor et al., 2004).  In a laboratory experiment, Saccharina latissima (studied as Laminaria saccharina) survived successfully between 17-32 psu (Druehl, 1967). However, Gerard & DuBois (1988) reported that Saccharina latissima had a salinity tolerance of 23-31 psu. Optimum growth rates in algae cultured from UK waters were achieved at 31 psu, while 16 psu dramatically decreased growth rates and 8 psu resulted in the death of the alga (Burrows & Pybus 1971).  In contrast, Saccharina latissima from the White Sea responded with decreased photosynthetic rates at 6-8 psu, while severe growth reductions were noted at 2 psu (Drobyshev, 1971).  Decreases in salinity to 5 psu for Saccharina latissima from Arctic Kongsfjorden (Spitsbergen) induced bleaching, indicative of cell damage after 5 days of incubation in the laboratory, while treatments decreasing from 20-10psu were associated with decreasing photosynthetic performance (Karsten, 2007). Juvenile sporophytes of Saccharina latissima can survive salinities of 13 for 3 weeks however, at 10 psu the juveniles become severely stressed and the majority die (Spurkland & Iken, 2011a).  In Arctic kelp, decreases in Saccharina latissima growth were associated with decreasing salinity (Spurkland & Iken 2011a).  Nielsen et al., (2014) also associated low growth, with decreases in salinity in a field experiment in Danish waters; while Weile (1996), recorded low growths (5.4 mm/day) in areas <14 psu. Responses of Saccharina latissima to salinity changes are population specific. Exposure to salinities outside a kelp’s tolerance range causes osmotic and ionic stress (Kirst 1990) resulting in decreased efficiency of their photosynthetic apparatus (<20-25%, Kirst & Wiencke, 1995).

Laminaria digitata tolerates a large salinity range within a 24 hour period (5-60psu; Karsten, 2007). Exposure to salinities outside a kelp’s tolerance range causes osmotic and ionic stress (Kirst 1990) resulting in decreased efficiency of their photosynthetic apparatus (<20-25, Kirst & Wiencke, 1995). At the extremes of Laminaria digitata’s salinity tolerance, decreases in photosynthetic rates are evident, particularly at low salinities (Gordillo et al., 2002).  On the Norwegian coast which is subjected to seasonal fluctuations in salinity, healthy Laminaria digitata plants were found growing at 15-25 psu (Sundene, 1964).  Laminaria digitata tolerates a large salinity range within a 24 hour period (5-60 psu; Karsten, 2007).  However, Birkett et al. (1998b) reported that all kelps are stenohaline species that required regular salinities of 30-35 psu to maintain optimum growth rates.  The associated biota are relatively tolerant to this changes in salinity, as most are typical of lower shore and sublittoral fringe biotopes. However, reduced salinty biotope have a lower species diversity, so some species may be lost due to a decrease in salinity at the benchmark level.

Sensitivity assessment. At the benchmark, a decrease in salinity from 'full' to 'reduced' (18-30 psu) for a year is unlikely to adversely affect Saccharina latissima or Laminaria digitata population, although their abundance may decrease slightly if growth rates are impaired.  However, if the changes were prolonged the associated flora and fauna may change, reflecting an increase in red algae and ascidians tolerant of reduced salinity.  In addition, while Laminaria digitata may tolerate reducced salinity conditions, it is replaced by Saccharina latissima in reduced salinity conditions, so that its abundance would probalby be uch reduced, and the so that the biotope may come to resemble IR.LIR.KVS.SlatPhyVS  or IR.LIR.KVS.SlatPsaVS.  However, at the benchmark level, IR.LIR.K.Slat.Ldig probably has a ‘High’ resistance to the pressure.  The biotope is considered to have ‘High’ resilience and hence 'Not sensitive' at the benchmark level.

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

Saccharina latissima is unlikely to be directly affected by this pressure at the prescribed benchmark. Increased competition from other species (such as Laminaria digitata)  with the change in environmental conditions will pose an indirect threat, as this biotope is defined by low levels of water movement, and Saccharina latissima thrives best in these conditions. Tidal streams of >0.5 m/s or lower as described by Connor et al. (2004).

Comparisons between biomass yields (dry weight) from two sites found significantly higher yields of Saccharina latissima at the moderately exposed site over the sheltered site, with light exposure and water velocity cited as the determining factors of both populations health (Peteiro & Freire, 2013). The turbulence created by friction at the frond-water interface acts as a transport mechanism for nutrients from the water column to the algae and is called the boundary layer. In conditions which lack water motion, the transportation of dissolved gases and nutrients within the boundary layer may be significantly reduced, leading to diminished growth (Wheeler, 1980, Parker, 1981, 1982); although conditions of no water motion are rare in the field (Gerard, 1982).  Water activity (wave, tidal and current mediated) may also be important for reducing sedimentation and the growth of filamentous algae which may compete with the key species in this biotope (Norton, 1978; Pihl et al., 1994; Isæus, 2004; Moy et al., 2006) and are the suggested reason for the absence of this biotope from extremely sheltered Norwegian waters (Bekkby & Moy, 2011). Despite this, populations of loose lying Saccharina latissima have been identified in areas of low water motion, in these conditions, attachment to the substratum does not appear to be important (Burrows, 1958); however if a lack of water movement results in a change in the kelp’s life history traits, this along with the likely change in associated species would be considered as equivalent to the loss of the biotope.

Saccharina latissima is absent from extremely sheltered conditions with little water flow in Norway.  This infers that Saccharina latissima needs a minimum amount of water movement in order to survive; perhaps because of decreased competition from filamentous algae and sedimentation, but also because water flow maintains a nutrient flux and enhances light penetration to juvenile sporophytes by moving the fronds (Norton, 1978; Pihl et al., 1995; Lobban & Harrison, 1994; Hurd, 2000; Isæus, 2004; Moy et al., 2006; Bekkby & Moy, 2011).  Decreased wave exposure also causes localised stagnation and de-oxygenation of the water column which would decrease survivorship in the area.

Saccharina latissima’s morphology was noted to differ between a moderately exposed and sheltered site, with those at the moderately exposed site exhibiting a large surface area than those at the sheltered site (Peteiro & Freire, 2013).  Kelps typically have a plastic morphology, in controlled laboratory experiments juvenile Saccharina latissima (studied as Laminaria saccharina) altered their morphology under different water flow exposures; mechanical longitudinal stress resulted in narrower blades of increased cell elongation, while a lack of tension lead to greater blade widths after 6 weeks (Gerard, 1987).  This plasticity is likely to protect thallus damage in areas of greater exposure or in stormier conditions. Stronger water currents may dislodge the kelp from bedrock or cause damage by moving boulders and cobbles.

However, Laminaria digitata forms dense forests in the fast flowing water of the rapids where water speeds vary from 4-6 knots (Bassindale et al., 1948). Laminaria digitata is also found in very strong flows (> 6 knots) although it is often out-competed by Alaria esculenta under these conditions. The biotope is not found in areas where sand scour occurs (associated with high water flow rates). Laminaria digitata partially achieves survival in a range of water flow conditions due to its blade morphology, which varies with flow, becoming narrower and more digitate as water flow rate increases (Sundene, 1964). As a result in increased water flow is likely to favour Laminaria digitata over Saccharina latissima.

Red algae are found in a range of water flow regimes, e.g. Delessaria sanguinea is recorded from moderately strong to weak tidal flows.  The ascidians are equaly found in a range of tidal flow, and good water flow is considered important for suspension feeders, depending on species. However, Clavelina lepadiformis thrives in areas where there is very little, if any, water movement (for instance, Abereiddy Quarry, Pembrokeshire (Hiscock & Hoare, 1975) and Ciona intestinalis is remarkably tolerant of low flow rates and is frequently found in areas with minimal water exchange and renewal such as harbours, marinas and docks.

Sensitivity assessment. This biotope is recorded from weak (>0.5 m/s) to negligible water flow in wave sheltered areas, so that wave meditated flow is also low.  The presence of Laminaria digitata in this biotope suggests that in condition of increased water flow it could out-compete Saccharina latissima, and thus change the identity of the biotope, especially in the shallow subtidal extent of the biotope.  A decrease in flow is not relevant as the biotope occurs in negligible flow. However, an increase in flow could result in loss of the biotope.  An increase in water flow of 0.1-0.2m/s for a year may be enough to change the relative abundance of Laminaria digitata and Saccharina latissima and change character of the biotope but unlikely to result in its loss within one year.  Therefore, a resistance of 'Medium' is suggested at the benchmark level. The resilience is probably 'High' so that this biotope is regarded as ‘Not sensitive’ at the benchmark level, although prolonged increase in flow could result in loss of the biotope.

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

This sublittoral fringe is dominated by predominantly sublittoral species. Air exposure causes desiccation prevents photosynthesis, and decreases growth rates in Saccharina latissima (studied as Laminaria saccharina, Kain, 1979). Kelps are generally less tolerant to desiccation than other brown macroalgae (e.g. Pelvetia canaliculata and fucoids) and are therefore likely to be competitively out-competed at their upper limits (Davison & Pearson, 1996, Harker et al., 1999). Laminaria digitata can survive water losses of 40% and is therefore considered moderately tolerant to desiccation. Laminaria digitata’s upper limits are set by competition with Fucus serratus (Hawkins & Harkin, 1985). Fucus serratus out-competes Laminaria digitata by controlling its respiration rates in tandem with its desiccation rates, allowing it to monitor and control water loss, which Laminaria digitata is unable to do.  An increase in emergence would lead to a depression in the upper limit of the biotope; while its lower limits may extend down the shore as irradiance levels increase in areas previously too deep for light-saturated photosynthesis to occur.

In conditions of low summer temperatures, both Saccharina latissima and Laminaria digitata have been documented as occurring in sheltered bays at the inner Porsangerfjord, North Norway, where the stands are completely drained at low tide (Sivertsen & Bjorge, 2015), suggesting that unique exceptions do exist in relation to this pressure, but are not the norm and are mediated by other environmental factors, e.g. temperature regime. this may explain why most records occur in Scottish waters. The associated red macroalgae of this biotope will have species specific responses to both increases and decreases in emergence with those of a saccate morphology generally more resistant to increased emergence than their counterparts (Oates, 1985, 1986).

Both kelp species are able to tolerate both an increased and decreased emergence; however this tolerance is based on the free movement of these species within their environmental optima, shifting their spatial extent up or down the shore. Therefore if an obstacle to movement perpendicular to the shore line (e.g. sea defence) is then combined with a change in the emergence regime this biotope could undergo compression of its range and may result in its local extinction. However in the footprint of the impact, a spatial shift of the biotope would result in the loss of the biotope, causing this biotope to be sensitive to the pressure at the benchmark.

Sensitivity Assessment. Emergence is a key driver of biotope extent because the upper and lower limits of Laminaria digitata are set by inter-species competition.  Additionally Saccharina latissima is likely to be less tolerant of increased emergence than its counterpart. In the case of a sea level rise, the change  may allow the biotope to shift up the shore, remaining within the sublittoral zone.  In the direct footprint of the impact resistance is therefore ‘None’ (loss of >75%). Resilience is suggested as ‘Medium’ (2-10 years) due to the scale of the impact, and suspected spatial relocation of the biotope under conditions of increased emergence and increased sea levels, provided there are no barriers to the biotope migration. 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

The occurrence of Saccharina latissima and therefore this biotope can be predicted by the level of wave action experienced by a location (Bekkby & Moy, 2011).  Saccharina latissima rarely grows in wave exposed conditions, as it is vulnerable to dislodgement from wave action and additionally may be attached to cobbles and boulders typical of this biotope, which may be overturned in conditions of increased wave action.  Increased wave exposure is also likely to detrimentally affect deposit feeders and species inhabiting the sediment which typically overlays the substratum in this biotope. In conditions of increased wave action Saccharina latissima may gradually change position, shifting into the lower eulittoral (Birkett et al., 1998b).   Competition from other species such as Laminaria digitata, able to withstand higher levels of wave action, may out-compete Saccharina latissima under natural conditions. Saccharina latissima has been cultivated in the presence of 6.4 m high waves (Buck & Buchholz, 2005), indicating that this competition is the likely driver of Saccharina latissima’s absence from exposed shores.  In conditions of greater wave action, Saccharina latissima productivity (studied as Laminaria saccharina) was less than that of sheltered population; this may have been due to greater nutrient availability in the sheltered site from a current of 0.5 meters/second/second (Gerard & Mann, 1979).  When considered in conjunction with emergence, wave exposure is beneficial to Saccharina latissima, with wave spray acting to hydrate individual alga which would otherwise suffer from desiccation and decreased growth rates (Kain, 1979).

While Saccharina latissima is generally absent from wave swept shores, it is also absent from extremely sheltered conditions in Norway.  Inferring that Saccharina latissima’s needs a minimum amount of water movement in order to survive; perhaps because of decreased competition from filamentous algae and sedimentation, but also because wave action maintains a nutrient flux and enhance light penetration to juvenile and smaller sporophytes by moving the fronds (Norton, 1978, Pihl et al., 1995, Lobban & Harrison, 1994, Hurd, 2000, Isæus et al., 2004, Moy et al., 2006 Bekkby & Moy, 2011).  Decreasing wave exposure also causes localised stagnation and de-oxygenation of the water column which would decrease survivorship in the area.

Sheltered conditions favour the growth of epiphytes, which decrease Saccharina latissima’s ability to withstand storm events and increased wave action, potentially increasing the vulnerability of this biotope to the pressure.  Growth of the epiphytic bryozoan, Membranipora membranacea reduces the ability of individual alga to withstand wave action, increasing frond breakages by making them brittle and reducing the maximum stress, toughness and extensibility of the kelp blade materials (Krumhansl et al., 2011).  Andersen, 2011 suggested that in conditions of increased wave activity, water movement may act to clear the fronds’ surface of epibiota, thus improving the health of the population in comparison to those in deeper and more wave sheltered areas.

The structure of kelp enables them to survive a range of wave conditions (Harder et al., 2006).   Comparisons between biomass yields from two sites found significantly higher yields at the moderately exposed site over the sheltered site, with light exposure and water velocity cited as the determining factors of both populations health (Peteiro & Freire, 2013).  The blades of Saccharina latissima at the moderately exposed site were also found to have a large surface area than those at the sheltered site.  Kelps typically have a plastic morphology, controlled laboratory experiments indicating that juvenile Saccharina latissima (studied as Laminaria saccharina) individuals alter their morphology under exposure to different water flow conditions, with mechanical longitudinal stress resulting in narrower blades of increased cell elongation while a lack of tension lead to greater blade width after 6 weeks (Gerard, 1987).  This plasticity is likely to protect thallus damage in areas of greater exposure or in stormier conditions, although stronger water currents may dislodge the kelp from bedrock or cause damage by moving boulders and cobbles.

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 >0.4 m; Gorman et al., 2013).  At medium to high levels of wave exposure, L.digitata biomass has been shown to decrease by 83% in the field (Wernberg & Thomsen, 2005). A flexible stipe and low profile holdfast allows Laminaria digitata to flourish in moderately to strongly wave exposed areas. A transplant experiment of Laminaria digitata, from exposed to sheltered sites resulted in a changed morphology with the frond widening, while individuals transplanted from sheltered to exposed sites became thinner more streamlined (Sundene, 1964; Gerard, 1987). This morphological plasticity is evident during the spore stage; because of this it is suggested that if wave height is increased or decreased the kelp will adapt morphologically over time to optimise its survival in the new environment. The associated assemblage of the biotope also influences Laminaria digitata’s ability to withstand increases in wave action. The encrusting of the epiphytic Membranipora membranacea which reduces the ability of individual kelp to withstand wave action, increasing frond breakages and additionally reducing the maximum stress, toughness and extensibility of the kelp blade materials (Krumhansl et al., 2011).

Sensitivity assessment.  This biotope is characteristic of wave sheltered to extremely wave sheltered conditions (Connor et al., 2004). The plastic nature of Saccharina latissima’s structure means that it is likely to withstand increase in wave exposure at the benchmark, however its fitness for the new environment will be diminished and it may not be able to out-compete other species including Laminaria digitata. This is likely to cause a shift in the biotope to those dominated by other kelp species through competition, especially at the shallow subtidal extent of the biotope.  Where increased wave action resulted in increase scour due to the mobility of coarse substrata (e.g. cobbles) then the biotope may become impoverished but Saccharina latissima remain the dominant kelp, as it is a rapid colonizing species, simlar to the IR.KIR.KwSed biotopes. Alternatively, where coarse sediment is absent, then Laminaria digitata may come to dominate.  However, a change of only 3-5% in significant wave height may not be significant even in such sheltered conditions. Therefore, the biotope probably has a resistance of 'Medium' to represent some changes in the relative abundance of kelp species.  Resilience is probably 'High', so that the sensitivity is probably 'Low'.

Transition elements & organo-metal contamination

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

Evidence

This pressure is Not assessed but evidence is presented where available.

Hydrocarbon & PAH contamination

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

Evidence

This pressure is Not assessed but evidence is presented where available.

Synthetic compound contamination

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

Evidence

This pressure is Not assessed but evidence is presented where available.

Radionuclide contamination

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

Evidence

No evidence

Introduction of other substances

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

Evidence

This pressure is Not assessed.

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

No direct evidence on the effects of deoxygenation for Saccharina latissima or Laminaria digitata were found in the literature, but reduced oxygen concentrations have been shown to inhibiting both photosynthesis and respiration in macroalgae (Kinne, 1977). Despite this, macroalgae are thought to buffer the environmental conditions of low oxygen, thereby acting as a refuge for organisms in oxygen depleted regions, especially if the oxygen depletion is short-term (Frieder et al., 2012).  A rapid recovery from a state of low oxygen is expected if the environmental conditions are transient. Additionally this biotope occurs in areas of low water movement.  If levels do drop below 4 mg/l, negative effects on these organisms can be expected with adverse effects occurring below 2mg/l (Cole et al., 1999).

Sensitivity Assessment.  Reduced oxygen levels are likely to inhibit photosynthesis and respiration but not cause a loss of the macroalgae population directly.  However, small invertebrate epifauna may be lost, causing a reduction in species richness. As the biotope is not considered dependent in any way upon these species and as these are not considered key characterizing species this loss is not considered in the sensitivity assessment. In additon, sublittoral fringe extent of the biotope is exposed to the air on extreme low tides  Therefore, based on Saccharina latissima and Laminaria digitata a resistance of ‘High’ is recorded.  Hence resilience is likely to be ‘High’, and the biotopes is probably ‘Not sensitive’ at the benchmark level.

Nutrient enrichment

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

Evidence

As a macroalgae, Saccharina latissima uptakes nitrogen and carbon from the water column in order to survive and grow.  The nitrogen and carbon content of Saccharina latissima varies annually, in conjunction with growth periods and nitrogen availability (Nielsen et al., 2014).  Carbon is used for winter growth and is stored during the summer as carbohydrate, while nitrogen is used for summer growth, and is a limiting factor (Nielsen et al., 2014).  High ambient levels of phosphate and nitrogen enhance spore formation in Saccharina latissima (Nimura et al., 2002), but will eventually inhibit spore production, particularly at the extremes of the alga’s temperature tolerance (studied as Laminaria saccharina; Yarish et al., 1990).  Saccharina latissima from the east coast of Scotland, showed increased growth rates in the laboratory when nutrient levels were enhanced by 25% (Conolly & Drew, 1985).  Enhancement of coastal nutrients is likely to favour those species with more rapid growth rates including turf forming algae (Gorgula & Connell, 2004). Epiphytic abundance and biomass on Laminaria longicruris for example increased under a eutrophic regime (Scheibling et al., 1999) and resulted in a shift from kelp dominated biotopes to an ephemeral algae dominated biotope in Norway (Moy & Christie, 2012).

A comparison of Laminaria digitata growth rates in Arbroath, Scotland with a more oligotrophic and a more eutrophic site appears to support the hypothesis that the growth of macroalgae in temperate coastal waters is generally limited by nitrogen in the summer period (Davison et al., 1984). In Helgoland, where ambient nutrient concentrations are double those of the Scotland site Laminaria digitata grows in the summer months. Laminaria digitata does not accumulate the significant internal reserves seen in some other kelps. Higher growth rates have also been associated with plants 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. Therefore, although nutrient enrichment may benefit Laminaria digitata, the indirect effects of eutrophication, such as increased light attenuation from suspended solids in the water column and interference with the settlement and growth of germlings, may be detrimental.

Sensitivity Assessment. The benchmark of this pressure (compliance with WFD ‘good’ status) allows for a slightly less diverse community of red, green and brown seaweeds with the greatest reduction in red species and an increase in the proportion of short lived species under the WFD criteria for good status.  The algae diversity in this biotope is already low with those remaining resistant to shading by kelp fronds and siltation. A further reduction in algal diversity would alter the biotope but would not result in loss of the biotope.  However, the biotope is considered 'Not sensitive' at the pressure benchmark that assumes compliance with good status as defined by the WFD.

Organic enrichment

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

Evidence

As a macroalgae, Saccharina latissima uptakes nitrogen and carbon from the water column in order to survive and grow.  The nitrogen and carbon content of Saccharina latissima varies annually, in conjunction with growth periods and nitrogen availability (Nielsen et al., 2014).  Carbon is used for winter growth, and is stored during the summer as carbohydrate, while nitrogen is used for summer growth (Nielsen et al., 2014).

The amount of organic nitrogen a Saccharina latissima stand may be able to uptake varies with location; with Saccharina latissima’s nitrogen uptake by a fish farm in Tristein, Central Norway estimated as 1.2 t of nitrogen per hectare of kelp over one growth season (Wang et al., 2014), while a similar setup in north-western Scotland predicted the removal of 5% waste nitrogen from 500 tonnes salmon over 2 years (Sanderson et al., 2012). The excrement and unused feed for fish farms increases the levels of organic matter in their local vicinity.  Evidence from experimental culture of Saccharina latissima around fish farms show enhanced growth rates by up to 61% at certain times in the year (Sanderson et al., 2012).  The quality of the nutrient source are also important with depressed growth rates associated with Saccharina latissima growing near a sewage sludge dumping ground in Liverpool Bay, Irish Sea (Burrows, 1971). 

A comparison of Laminaria digitata growth rates in Arbroath, Scotland with a more oligotrophic and a more eutrophic site appears to support the hypothesis that the growth of macroalgae in temperate coastal waters is generally limited by nitrogen in the summer period (Davison et al., 1984). In Helgoland, where ambient nutrient concentrations are double those of the Scotland site Laminaria digitata grows in the summer months. Laminaria digitata does not accumulate the significant internal reserves seen in some other kelps. Higher growth rates have also been associated with plants 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. Therefore, although nutrient enrichment may benefit Laminaria digitata, the indirect effects of eutrophication, such as increased light attenuation from suspended solids in the water column and interference with the settlement and growth of germlings, may be detrimental.

Sensitivity assessment. At the benchmark level (a deposit of 100gC/m²/yr) this biotope could be resistant to the pressure, as suggested by the survival and enhanced growth of Saccharina latissima near fish farms and Laminaria digitata near sewage outfalls, associated with high levels of organic matter. Resistance to this pressure is therefore regarded as ‘High’, although beyond the benchmark, negative consequences of enhanced organic enrichment are possible.  Resilience is therefore also regarded as ‘High’ and the biotope is therefore probably ‘Not sensitive’ at the pressure benchmark.

Physical loss (to land or freshwater habitat)

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

Evidence

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

Physical change (to another seabed type)

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

Evidence

Sensitivity assessment.  Laminaria digitata requires stable hard substratum for attachment. A change in substratum type from bedrock to sedimentary would render the habitat unsuitable because kelp requires a stable substratum on which to settle. Saccharina latissima can occur on sediment where enough large pebbles, cobbles or boulder occur to provide attachment.  No evidence of this biotope occurring on sedimentary substratum was found in the literature (see SS.SMp.KSwSS biotopes).  However, a change in seabed type would change the character of the biotope from rock biotope to a sedimentary biotope, so that Laminaria digitata and many of the red seaweed community would be or replaced. The biotope would be lost so that resistance is ‘None’ to this pressure. As the pressure is permanent, resilience is 'Very low' and hence the sensitivity is likely to be 'High'. 

Physical change (to another sediment type)

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

Evidence

Not relevant to bedrock biotopes

Habitat structure changes - removal of substratum (extraction)

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

Evidence

The species characterizing this biotope are epifauna or epiflora occurring on rock and would be sensitive to the removal of the habitat. However, extraction of rock substratum is considered unlikely and this pressure is considered to be ‘Not relevant’ to hard substratum habitats.

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

No direct evidence was found for this pressure on this biotope.  Low-level disturbances (e.g. solitary anchors) are unlikely to cause harm to the biotope as a whole, due to the impact’s small footprint.  Natural abrasion of the lamina tips occurs continuously, even in calm conditions (Krumhansl, 2012) as a result of water friction, although this erosion may be beneficial to the plants, reducing drag on the thalli (Reed et al., 2008, Krumhansl & Scheibling, 2011; Gunnill, 1985).  While Saccharina latissima is usually permanently attached to the substratum, Burrows (1958) suggests that re-attachment to the substratum after dislodgement is possible with individuals regrowing hapteron branches. It is, therefore, possible that individuals may be able to withstand dislodgement and abrasion. Survival of Saccharina latissima in areas where high levels of abrasion occur (a glacial influenced shore) indicate the phenotypic plasticity of the species and suggest that this species, and therefore the habitat, may be resistant to a higher degree of abrasion than other kelp biotopes (Spurkland & Iken, 2011a). Additionally, Saccharina latissima was the only kelp species present on an exposed glacial shore, where high levels of abrasion, inorganic sediment and siltation occurred, while an adjacent sheltered site boasted five kelp species (Spurkland & Iken, 2011b).

In a review of the effects of trampling on intertidal habitats, Tyler-Walters & Arnold (2008) found no information on the effects of trampling on Laminaria species (Laminaria digitata and Laminaria saccharina). The authors suggested that laminarians are robust species but that trampling on blades at low tide could potentially damage the blade or growing meristem. Trampling on shallow algal communities in the Mediterranean reported that erect canopy forming species (e.g. Cysterseira spp., Dictyota spp.) were the worse affected, and suffered a reduction in abundance but were reduced to just holdfasts at high trampling intensities (Milazzo et al., 2002; Tyler-Walters, 2005).

Sensitivity assessment. There is little evidence on sensitivity to abrasion in this biotope. Abrasion via trampling could damage parts of the adult kelp and red algae and lead to the removal of individuals.  Abrasion by passing bottom trawls or similar gear may remove or damage large erect kelps, and the associated biological assemblage could also be damaged, dislodged or killed. Therefore, a resistance of ‘Low’ is suggested based on limited evidence.  The resilience is probably 'High', and sensitivity is, therefore, 'Low'.

Penetration or disturbance of the substratum subsurface

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

Evidence

The species characterizing this biotope group are epifauna or epiflora occurring on hard rock, which is resistant to subsurface penetration.  Therefore, ‘penetration’ is 'Not relevant'. The assessment for abrasion at the surface only is, therefore, considered to equally represent sensitivity to this pressure’. Please refer to ‘abrasion’ above.

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

Next to wave exposure, light was a key descriptor of Saccharina latissima’s distribution along the Norwegian coast, indicating its importance to this biotope’s identity (Bekkby & Moy, 2011). This biotope typically occurs in silty conditions, with Saccharina latissima able to maintain a positive carbon budget in very low light conditions (Andersen et al., 2011). As a photosynthetic organism, ultimately Saccharina latissima’s depth distribution is reliant on light availability (Lüning, 1979; Lüning & Dring, 1979; Gerard, 1988).  Therefore, an increase in turbidity may lead to the mortality of algae at the biotope’s deeper range limit and may limit the biotope to shallower waters.

Blue light is crucial for the gametophytic stages of Saccharina latissima, and several other congenic species (Lüning, 1980).  Without blue light (1-4 nE cm/s) and in the presence of red light, female gametophytes do not become fertile or produce eggs (Lüning & Dring, 1975). In comparison to Laminaria digitata and Laminaria hyperborea, Saccharina latissima exhibits a higher level of tolerance to UV light (indicative of its opportunistic nature, 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. Populations of Saccharina latissima’s exhibit different rates of carbon assimilation and growth when exposed to different light acclimation levels in laboratory conditions with alga from turbid sites possessing the fastest growth across treatments (Gerard, 1988).  Deep water populations also exhibit adapted characteristics, with daily irradiances exceeding an average of 20 E (radiant flux) /m² /day reduce growth rates. The tolerance of a particular population to this pressure must, therefore, be considered in isolation.

Decreases in suspended solids are initially likely to increase photosynthesis and productivity of Saccharina latissima. However, in conditions of greater water clarity (reduced suspended solids) Laminaria digitata typically out-competes Saccharina latissima, resulting in the loss of the biotope (Norton, 1978).  An absence of this biotope in low silt environments is therefore expected, although, with greater water clarity, it may be able to shift its range to deeper waters.

Increases in the levels of suspended sediment were found to reduce growth rates in Saccharina latissima (studied as Laminaria saccharina) by 20% (Lyngby & Mortensen, 1996). Suspended Particle Matter (SPM) concentration has a linear relationship with subsurface light attenuation (Kd) (Devlin et al., 2008).  Laminaria spp. show a decrease of 50% photosynthetic activity when turbidity increases by 0.1/m (light attenuation coefficient = 0.1-0.2/m; Staehr & Wernberg, 2009). 

Burrow & Pybus (1971) found that the mean thalli thickness of Saccharina latissima (studied as Laminaria saccharina) that had grown in the silted waters of Redcar, Souter Point and Robin Hood's Bay (North-East England) were significantly smaller than those grown in the clearer waters of St Abbs (North-East England) and Port Erin (Isle of Man). Because of the low water movement associated with this biotope, suspended solids are not likely to be removed by water currents or turbulence and subsequent siltation of the biotope is, therefore, likely. Decreases in siltation may also cause a shift in the identity of the associated assemblage, as suspension and deposit feeders receive fewer nutrients, due to the lower carbon input and suspension feeders benefit as their feeding apparatus suffer less from clogging by silt. Red algae are shade tolerant so less sensitive to a reduction in light than the kelp species, although the increased siltation and scour may be detrimental to the less robust species. 

Sensitivity assessment. A decrease in suspended particulates from e.g. intermediate to clear (see benchmark) is likely to reduce siltation and scour, and allow Laminaria digitata)  to increase in abundance, especially at the shallow subtidal extent of the biotope with a resultant change in the character of the biotope. The biotope is likely to be replaced by mixed kelp biotopes, depending on the extent of the change in suspended solids and the presence of mobile coarse sediments.  An increase in turbidity at the benchmark e.g. from clear to intermediate represents a change from 0.67 to 6.7 in light attenuation coefficient (extracted from Devlin et al., 2008), and a change from intermediate to turbid conditions is considerably greater.  Based on the observation that Laminaria sp. show a 50% decrease in photosynthetic activity after a change in light attenuation of only 0.1/m it is likely that the growth of Saccharina latissima and Laminaria digitata would be significantly decreased.  In addition, Laminaria digitata has a lower level of tolerance to suspended solids than Saccharina latissima. Therefore, an increase in suspended solid is likely to remove Laminaria digitata and change the composition of the red algal community due to increased scour. Although the effects of light attenuation may be reduced in the sublittoral fringe where the biotope is emersed for short periods of time, the abundance Saccharina latissima is also likely to decline, resulting in a change in the biotope. Therefore, resistance to decreased and increased turbidity is likely to be  ‘Low’. Resilience is probably  ‘High’. The biotope, therefore, has ‘Low’ sensitivity to the pressure.

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

Low levels of siltation have been shown to initially offer protection to Saccharina latissima from UVR in laboratory experiments with thallus samples (Roleda et al., 2008).  However, after burial under a variety of sediment types, for over 7 days, symptoms of degradation, bleaching, tissue loss and reduced PSII function, were evident (Roleda & Dethleff, 2011).  Laboratory experiments show that even a very thin deposit of fine grained sediment (0.1 -0.2 cm thick) caused rotting of Saccharina latissima, resulting in 25% mortality if covered for 4 weeks, under conditions of no water movement (Lyngby & Mortensen 1996). In the field, these conditions (no water movement) rarely exist and might explain the survival of Saccharina latissima sporophytes in areas of siltation (Birkett et al., 1998b). 

The gametophytic and zoospore stages are more vulnerable than their adult counterpart.  Laboratory experiments indicated the adverse effects of siltation on Saccharina latissima, including abnormal development of the zoospore (Burrows, 1971). Other studies have indicated that siltation inhibits spore settlement with spores failing to form attachments to the fine sediment or the hard bedrock beneath, resulting in their subsequent loss from the biotope by water activity (Devinny & Volse, 1978, Norton, 1978; Bartsch et al., 2008).  Laminaria digitata is more sensitive to this pressure than other subtidal brown algae (e.g. Sargassum muticum; Morrell & Furnham, 1982). Therefore, a smothering event may favour Saccharina latissima, which may allow it to out-compete Laminaria digitata and change the biotope’s identity. 

However, smothering of the whole sporophyte is unlikely to last for long, if deposition is light (<5 cm) silt is likely to fall from the fronds to the substratum, even in conditions of weak water movement, therefore the rates of photosynthesis and growth are likely to return to normal within a few days of the deposition event.  Also, the characteristic kelps are large and unlikely to adversely affected by smothering by 5 cm sediment unless the deposition occurred at low tide.  The understorey of red algae and fucoids may experience some mortality but the character of the biotope is unlikely to change.

Sensitivity assessment. Where smothering is short-term (less than 7 days), then this biotope should be relatively resistant.  This biotope is recorded from low energy habitats (wave sheltered and weak tidal streams) deposited sediment may remain for some time, depending on the local conditions and topography.  Nevertheless, a resistance of 'High is suggested, although long-term smothering would be detrimental. The resilience of the biotope is considered to be ‘High’ and the sensitivity of this biotope is, therefore ‘Not sensitive' at the benchmark, although confidence is low and local hydrography may increase or decrease the resistance.

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

Low levels of siltation have been shown to initially offer protection to Saccharina latissima from UVR in laboratory experiments with thallus samples (Roleda et al., 2008).  However, after burial under a variety of sediment types, for over 7 days, symptoms of degradation, bleaching, tissue loss and reduced PSII function, were evident (Roleda & Dethleff, 2011).  Laboratory experiments show that even a very thin deposit of fine grained sediment (0.1 -0.2 cm thick) caused rotting of Saccharina latissima, resulting in 25% mortality if covered for 4 weeks, under conditions of no water movement (Lyngby & Mortensen 1996). In the field, these conditions (no water movement) rarely exist and might explain the survival of Saccharina latissima sporophytes in areas of siltation (Birkett et al., 1998b). 

The gametophytic and zoospore stages are more vulnerable than their adult counterpart.  Laboratory experiments indicated the adverse effects of siltation on Saccharina latissima, including abnormal development of the zoospore (Burrows, 1971). Other studies have indicated that siltation inhibits spore settlement with spores failing to form attachments to the fine sediment or the hard bedrock beneath, resulting in their subsequent loss from the biotope by water activity (Devinny & Volse, 1978, Norton, 1978; Bartsch et al., 2008).  Laminaria digitata is more sensitive to this pressure than other subtidal brown algae (e.g. Sargassum muticum; Morrell & Furnham, 1982). The literature suggests that Laminaria digitata is sensitive to prolonged smothering (Roleda & Dethleff,  2011). Therefore, a smothering event may favour Saccharina latissima, which may allow it to out-compete Laminaria digitata and change the biotope’s identity. 

Sensitivity Assessment.  While a light covering may fall from fronds and be transported from the biotope relatively quickly, a deposition of 30 cm is likely to remain in place and therefore have a greater effect on the biotope, potentially resulting in the death of Saccharina latissima and therefore the loss of the biotope. Laminaria digitata may be tall enough to escape direct smothering of the thallus but smothering of the stipe and holdfast may result in deoxygenation and rot, and/or scour. Smothering of the associated epifauna and flora may also result in mortality, depending on the how long the deposit remained over the biotope.  This biotope is regarded as having ‘Low’ resistance. Since the biotope occurs in conditions of low water movement, the natural removal of sediment from the biotope is likely to be slow or non-existent. Resilience to this pressure is therefore regarded as ‘Medium’  Sensitivity to this pressure is therefore also assessed as ‘Medium’ although confidence is low and local hydrography may increase or decrease the resistance.

Litter

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

Evidence

Not assessed. It is feasible that discarded fishing line, plastic netting, or similar discards could tangle on kelp fronds and potentially damage or remove individuals.  However, no doucmented evidence was found.

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

Next to wave exposure, light was a key descriptor of Saccharina latissima’s distribution along the Norwegian coast, indicating its importance to this biotope’s identity (Bekkby & Moy, 2011). This biotope typically occurs in silty conditions, with Saccharina latissima able to maintain a positive carbon budget in very low light conditions (Andersen et al., 2011). As a photosynthetic organism, ultimately Saccharina latissima’s depth distribution is reliant on light availability (Lüning, 1979; Lüning & Dring, 1979; Gerard, 1988).  Therefore an increase in turbidity may lead to the mortality of algae at the biotope’s deeper range limit and may limit the biotope to shallower waters.

Blue light is crucial for the gametophytic stages of Saccharina latissima, and several other congenic species (Lüning, 1980).  Without blue light (1-4 nE cm/s) and in the presence of red light, female gametophytes do not become fertile or produce eggs (Lüning & Dring, 1975). In comparison to Laminaria digitata and Laminaria hyperborea, Saccharina latissima exhibits a higher level of tolerance to UV light (indicative of its opportunistic nature, 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. Populations of Saccharina latissima’s exhibit different rates of carbon assimilation and growth when exposed to different light acclimation levels in laboratory conditions with alga from turbid sites possessing the fastest growth across treatments (Gerard, 1988).  Deep water populations also exhibit adapted characteristics, with daily irradiances exceeding an average of 20 E (radiant flux) /m² /day reduce growth rates. The tolerance of a particular population to this pressure must, therefore, be considered in isolation.

Increases in the levels of suspended sediment were found to reduce growth rates in Saccharina latissima (studied as Laminaria saccharina) by 20% (Lyngby & Mortensen, 1996). Suspended Particle Matter (SPM) concentration has a linear relationship with sub surface light attenuation (Kd) (Devlin et al., 2008).  Laminaria spp. show a decrease of 50% photosynthetic activity when turbidity increases by 0.1/m (light attenuation coefficient = 0.1-0.2/m; Staehr & Wernberg, 2009). Therefore any activity that decreases incident light (e.g. shading) may be detrimental.

Sensitivity assessment. An increase in incident light is likely to increase plant productivity and increase the density of the kelps. However, there is no evidence that artificial light sources have caused an increase in macroalgal productivity. Constant artificial light may affect the reproductive cues, development of gametophytes etc, but no evidence was found.  However, shading, especially from permanent structures (e.g pontoons, jetties) are likely to reduce incident light, and will probably result in the reduction in kelp density, or even its exclusion from the affected area. Therefore, a resistance of 'Low' is suggested. Resilience is probably 'High' if the shading is temporary but 'Very low' if permanent. Therefore, a precautionary sensitivity of 'High' is suggested.

Barrier to species movement

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

Evidence

Not relevant – this pressure is considered applicable to mobile species, e.g. fish and marine mammals rather than seabed habitats.  Barriers to propagule (larvae, zoospores) supply could adversely affect the population because it is dependent on rapid recolonization after disturbance. However, most of the community, including the kelps, are widespread and also may be self-recruiting within the habitat or between adjacent habitats. Any permanent structures that completely block water exchange would be detrimental but mainly due to the permanent change in hydrography.  No evidence of direct impacts was found.

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

Injury or mortality from collisions of biota with both static and/or moving structures is most relevant to mobile species. Intertidal habitat may be damaged due to grounding of vessels (boats, ships, tankers etc), and is addressed under 'abrasion' above.

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 evidence regarding the genetic modification of key characteristic species was found. Cultivation of this species is becoming more common and may be achieved in coastal waters far from shore, increasing the species’ potential larval dispersal range.  There is a high degree of plasticity within Saccharina latissima, as indicated by Gerard (1988) suggesting that this species would be resistant to the introduction of genetically modified populations. No evidence that Saccharina latissima cross-breeds with any of its congenic species was found. Cultivation of this species from translocated individuals does occur, however, the effects of this process on the natural populations of this species are not known (Peteiro et al., 2014).

Harvesting is carried out on wild kelp stands in a sustainable 5 year cycle (Vea and Ask, 2011), therefore, translocation of species is unlikely.  Additionally if translocation of populations does occur, a loss in genetic diversity is not regarded as an issue for Laminaria digitata, unless additional pressures result in the isolation and fragmentation of wild coastal populations (Valero et al., 2011). Genetic differentiation in wild populations occurs within 10 km with genetic flow occurring between adjacent species (Billot et al., 2003).  No evidence that Laminaria digitata cross-breeds with any of its sister species was found. 

Sensitivity assessment. No direct evidence was found that might indicate the effects of this pressure on the biotope. Inter-breeding between populations occurs in most Laminaria species; therefore the resistance of this biotope to the pressure may be ‘High’, with ‘High’ resilience. Sensitivity for this pressure is also suggested as ‘Not sensitive’.

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 spp. tormentosoides. In Nova Scotia, Codium fragile spp. tormentosoides 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 spp. tormentosoides prevents re-colonization by other macro-algae (Scheibling & Gagnon, 2006).  The grazer, Lacuna vincta preferentially grazes on Saccharina latissima over the invasive macroalgae Codium fragile in the Gulf of Maine, USA (Chavanich & Harris., 2004).  If similar conditions exist in UK waters, where native grazers preferentially feed on the native Saccharina latissima, then the invasive species will have an initial advantage, and may potentially out-compete Saccharina latissima, leading to the loss of the biotope.

The survival of Saccharina latissima in harbours and docks despite heavy fouling by epibionts has been documented in the southwest of England (Johnston et al., 2011), while the health of this kelp is undetermined; their presence illustrates the resilience of this biotope against this pressure. However, if Saccharina latissima is out-competed by invasive macroalgae, its recolonization could be prevented by heavy fouling of non-native origin, in a similar way that native fouling organisms have prevented re-colonization and recovery of Saccharina latissima beds in the Skagerrak area (Andersen et al., 2011).

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 and 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 0-0.5 m or 4-6 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; Hieser et al., 2014; Arnold et al., 2016; Epstein & Smale, 2017; Epstein & Smale, 2018; Kraan, 2017; Epstein et al., 2019a,b; Tidbury, 2020). Undaria pinnatifida originates from Japan but is established currently on the coastlines of New Zealand, Australia, Northern France, Spain, Italy, the UK, Portugal, Belgium, Holland, Argentina, Mexico, and the USA (De Leij et al., 2017). Undaria pinnatifida was first recorded in the UK in the Hamble Estuary in 1994 (Macleod et al., 2016) and 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). De Leij et al. (2017) suggested that in natural substrata, Undaria pinnatifida can be inhibited by the presence of native competitors, such as large perennial species. The dense macroalgae canopies formed by native kelps result in limited space and light availability for Undaria pinnatifida recruits. However, it will not always completely prevent the assimilation of Undaria pinnatifida (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 has a greater preference for sites sheltered 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 Plymouth Sound (UK), Epstein et al. (2019b) found that within its depth range (+1 to –4 m), Undaria pinnatifida co-existed with seven species of canopy-forming brown macroalgae, including Saccharina latissima and Laminaria digitata. However, they reported that Undaria pinnatifida biomass was negatively related to Saccharina latissima in both intertidal and subtidal habitats. This was only statistically significant in subtidal habitats, which suggested that there was some competition between the two species (Epstein et al., 2019b).

Heiser et al. (2014) surveyed 17 sites within Plymouth Sound, UK and found that Saccharina latissima was significantly more abundant at sites with Undaria pinnatifida with ca 5 Saccharina latissima individuals present per m², compared to ca 0.5 Saccharina latissima individuals per m² present at sites without Undaria pinnatifida.

Undaria pinnatifida has been reported to both co-exist with and out-compete Saccharina latissima (Farrell & Fletcher, 2006; Heiser et al., 2014; Epstein et al., 2019b). For example, in Torquay Marina, UK, Farrell & Fletcher (2006) completed a canopy removal experiment between 1996-2002. They reported that Saccharina latissima decreased in both control and treatment plots from ca 3 plants per 0.45 m² in 1996 to ca 1 plant per 0.45 m² in 1997 and had disappeared completely from pontoons by 2002. This coincided with a significant increase in Undaria pinnatifida from zero plants per 0.45 m² in 1996 to ca 6 plants per 0.45 m² in 1997. However, there was a slight decrease in Undaria pinnatifida in both control and treatment plots between 1997 and 1998. By 2002, Undaria pinnatifida had recovered at control and treatment plots to ca 4-6 plants per 0.45 m² whereas Saccharina latissima had not.

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). Full removal of the existing kelp in Plymouth Sound canopy allowed the mean cover of Undaria pinnatifida to increase following a full canopy removal experiment from ca 10% to ca 50% within three months De Leij et al. (2017). Their experiment showed that the density of Laminaria digitata was important to Undaria pinnatifida invasion (De Leij et al., 2017).

Similarly, a primary succession experiment by Epstein et al. (2019b) in Plymouth Sound (UK) showed that clearance of Laminaria digitata in 2016 resulted in an increase in Undaria pinnatifida. However, this was quickly followed by the recovery of Laminaria digitata in 2017 and a concurrent decline in Undaria pinnatifida, suggesting that Laminaria digitata had a higher fitness (Epstein et al., 2019b). Within the same study, Epstein et al. (2019b) observed that on rocky reef substrata, Undaria pinnatifida exhibited a significant negative relationship with Laminaria digitata in intertidal habitats, suggesting that Laminaria digitata negatively affects Undaria pinnatifida abundance. It was also suggested that Undaria pinnatifida has a lower resistance to desiccation than Laminaria digitata.

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. 

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 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 that is 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 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).

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 and Sargassum muticum can co-exist with native kelp species within its depth range (-1 to 4 m) e.g. Laminaria digitata and Saccharina latissima as shown in Plymouth Sound and Stangford Lough, respectively. A dense kelp canopy may restrict or slow the proliferation of Undaria pinnatifida or Sargassum muticum.  But, Laminaria digitata has been shown to out-compete Undaria pinnatifida.  For example, the removal of the Laminaria digitata canopy increased Undaria pinnatifida abundance but the recovery of Laminaria digitata in the following year resulted in a concurrent decline in Undaria pinnatifida.

This biotope (IR.LIR.K.Slat.Ldig) occurs in low energy environments with a full or variable salinity in the sublittoral fringe or lower shore, which are the preferred habitat conditions for Undaria pinnatifida and Sargassum muticum. This biotope also has a mixed kelp canopy of Saccharina latissima and Laminaria digitata may inhibit the colonization of Undaria pinnatifida but any disturbance may allow Undaria to colonize. 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. However, Undaria may out-compete Saccharina latissima. A significant reduction in the abundance of Saccharina latissima will result in different mixed kelp canopies including Undaria and result in loss of the biotope as defined in the classification.  However, Sargassum muticum also prefers wave sheltered, shallow sites in the sublittoral fringe, and has been reported to invade and out-compete Laminaria digitata in kelp beds in France (Cosson, 1999; de Bettignies et al., 2021).

Therefore, resistance is assessed as ‘Low’ due to the potential loss of Saccharina latissima and Laminaria digitata. While Laminaria digitata may out-compete Undaria the recovery after invasion by Sargassum, although rapid, would require direct intervention (removal) so that resilience is assessed as ‘Very low’. Hence, the 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. However, it has been recorded in similar kelp habitats in Norway (Järnegren et al., 2023). Didemnum vexillum requires hard substrata for successful colonization, therefore, it could colonize the bedrock and boulders that characterize this biotope. Also, Didemnum vexillum prefers wave-sheltered conditions and has been recorded in the lower intertidal. Didemnum vexillum can overgrow sessile organisms, including kelp Laminaria sp. However, no direct evidence was found on how Didemnum vexillum affects kelp or if it contributes to Laminaria sp. mortality, although epifaunal growth by Membranacea membrancea was reported to reduce the physical strength of kelp fronds (inc. Laminaria digitata) and make them susceptible to removal by wave action (Krumhansl et al., 2011). In addition, overgrowth by epiphytes contributed to the decline of Saccharina latissima in Norway (Andersen et al., 2011). However, Didemnum vexillum may compete for light and space with kelp and epifauna and could interfere with recruitment, which could lead to the mortality of some epifauna, the loss of kelp, and a reduction in biodiversity. Therefore, a resistance of 'Medium' (some mortality, <25%) is suggested as a precaution. 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 'Medium'.

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

Little direct evidence was found in the literature with only two studies found on microscopic algal pathogens. Saccharina latissima (studied as Laminaria saccharina) may be infected by the microscopic brown alga Streblonema aecidioides which may manifest to different degrees from dark spots to heavy deformations and crippled thalli and reduce growth rates.  Infection rates have been recorded as 87% (±13%) in Kiel Bay, Western Baltic (Peters & Scaffelke, 1996).   Association of Saccharina latissima with a marine bacterium, Pseudomonads in the Baltic Sea protects the algae from 2 algal pathogens, Pseudoalteromonas elyakovii and Algicola bacteriolytica. Pseudomonads produces antibiotics which prevent Saccharina latissima’s infection, suggesting that this biotope’s resistance to disease is population and location specific (Nagel et al., 2012).  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).  No evidence was found regarding introduction of pathogens or metazoan disease vectors to kelp biotopes.

Sensitivity Assessment. Due to the evidence for resistance, biotope continuation under a high pathogen load, and the evidence of disease resistance in kelps, resistance to this pressure is regarded as ‘High’ and resilience is therefore also ‘High’. Hence ‘Not sensitive’ is recorded.

Removal of target species

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

Evidence

In the UK, harvesting of Saccharina latissima is confined to manual harvesting on a small scale, and farming. Manual harvesting may involve individual blade or whole alga removal. Only two seaweed leases exist in the UK illustrating the low impact of this species’ harvesting in the wild in UK waters. Mechanical harvesting of Saccharina latissima is done in Italy, but the preferred method of commercial harvesting in Europe is by farming on ropes (Seaweed Industry in Europe, Netalgae, 2012).  Low level removal of individuals from the shoreline is unlikely to have an effect on the local biotope, however if harvesting of wild Saccharina latissima increased, the time window for harvesting (Low tide) is relatively small and could act as a buffer against excessive harvesting of the species. However if gathering by diving also increased there would be little resistance to the pressure. Associated species are unlikely to be affected by low level removal of Saccharina latissima unless protection from desiccation on the lower shore is important.

Overfishing of apex predators (in particular fin fish), has been occurring for centuries in UK and Irish waters, resulting in habitats dominated by invertebrates and commercially undesirable fish such as the lesser spotted catshark (Molfese et al., 2014) suggesting an ecosystem level shift in the functioning of these food webs. The urchin barrens recorded off the coast of Norway and in the North West Atlantic, are not common to UK waters with deforestation by urchins instead restricted and patchy and could be a result of this shift, leading to a temporally more stable, less dynamic biotope (although some have been noted in Scotland; Smale et al., 2013).

Unlike Saccharina latissima, Laminaria digitata is mechanically harvested in Europe, particularly in Brittany, France; although it is only harvested manually or by farming in the UK (Seaweed Industry in Europe, Netalgae, 2012). 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).

Debate exists on whether kelp harvesting is detrimental to fish stocks. While some state that no negative consequences of harvesting have been documented (Vea and Ask, 2011); others suggest that as important foraging and nursery grounds for birds and fish, removal will inevitably result in negative consequences (Lorentsen et al.,2010). 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). Conflicts in the literature may arise from the comparisons of different fisheries. Maintaining a sustainable crop of Laminaria digitata has been suggested as 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 has been indicated as a threat to the continued harvesting effort of Laminaria digitata (Engelen et al., 2011).

Sensitivity assessment. Saccharina latissima is harvested via on aquaculture rather than wild harvesting. However, Laminaria digitata could be harvested from wild beds.  Therefore, if harvesting of the species occurred extensively in an area then there would be little resistance to the pressure. Resistance is regarded as ‘None’ as the pressure is defined as the removal of key characterizing species from the biotope. Resilience to this pressure is probably ‘Medium’. Sensitivity to this pressure is defined as ‘Medium’.

Removal of non-target species

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

Evidence

No direct evidence was found for the removal of Saccharina latissima or Laminaria digitata from a biotope as by-catch. However if they were removed as by-catch, the result would be the loss of the biotope. 

Sensitivity assessment. Resistance to this pressure is considered ‘Low’ as removal of the structuring species would significantly alter the character of the biotope. Resilience is therefore assessed as 'High’ and sensitivity ‘Low’.