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 Spitsbergen (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 months at 15°C (Lüning, 1988).

The life cycle of kelps is 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 the future settlement of Saccharina latissima slowing or stopping recovery of the biotope (Moy & Christie, 2012).

Increased temperatures bring with them increased the 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 epiphytic loading enhances blade tissue loss (Andersen et al., 2013).  If environmental conditions for spore survival are not favourable, then the 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. The 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 the 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.

Bishop (1985) noted that gametogenesis of Echinus esculentus proceeded at temperatures between 11-19°C although continued exposure to 19°C destroyed synchronicity of gametogenesis between individuals. Embryos and larvae developed abnormally after up to 24 hr at 15°C (Tyler & Young, 1998). Bishop (1985) suggested that Echinus esculentus could not tolerate high temperatures for prolonged periods due to increased respiration rate and resultant metabolic stress.

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 for that year depending on when the increase occurs because sporogenesis in Saccharina latissima requires a minimum period of 4 weeks at or below 15°C combined with short day lengths. 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. The red algae community may survive a 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. Echinoderms most of the subtidal echinoderms are probably stenothermal and will avoid increases in temperature. Therefore, the resistance of this biotope to an increase in temperature is assessed as ‘Medium’. Resilience is likely to be ‘High’ and sensitivity, therefore ‘Low’.

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 Spitsbergen (Van den Hoek & Donze, 1967, Lüning, 1990). Its distribution suggests that the species would tolerate a chronic temperature change (e.g. by 2°C for a year).  Other associated organisms to this biotope may fair less well.  The urchin Psammechinus miliaris was adversely affected by the 1962/63 winter, while the crinoid (rosy feather star) Antedon bifida may have been lost from the Menai Straits following winter 1947 (D.J. Crisp pers. comm. to K. Hiscock).

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). 

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 2°C for one year.  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

Both IR.LIR.K.Slat.Ft and IR.LIR.K.Slat.Pk are recorded from full salinity conditions but Saccharina latissima is also typical of variable or 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 20-10psu were associated with decreasing photosynthetic performance (Karsen, 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 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).  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).  Neilsen 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).

The associated biota are relatively tolerant to this changes in salinity, Delesseria sanguinea tolerates salinities of 11 psu in the North Sea, while the brittle star Ophiothrix fragilis occurs at salinities of 10-16 psu (Wolff, 1968). Associated echinoderms are likely to fair less well as they don’t possess an osmoregulatory organ (Boolootian, 1966). At low salinities, urchins gain weight, and the epidermis loses its pigment; prolonged exposure is fatal. The coelomic fluid of Echinus esculentus is isotonic with seawater (Stickle & Diehl 1987). Because of this, a decrease in salinity within the benchmark may result in lowering the grazing pressure on the biotope and, may in the short-term be beneficial to the biotope.

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 population up to ca 55 psu (Karsten, 2007).  Little evidence for the effects of hypersaline conditions on the associated flora and fauna was found, although most echinoderms are generally regarded as stenohaline (Russell, 2013). Therefore, the resistance is probably 'Medium' to represent the potential loss of members of the associated flora and fauna. Resilience is 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

Both IR.LIR.K.Slat.Ft and IR.LIR.K.Slat.Pk are recorded from full salinity conditions but Saccharina latissima is also typical of variable or 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 (Karsen, 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).  Neilsen 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).

The associated biota are relatively tolerant to this changes in salinity, Delesseria sanguinea tolerates salinities of 11 psu in the North Sea, while the brittle star Ophiothrix fragilis occurs at salinities of 10-16 psu (Wolff, 1968). Associated echinoderms are likely to fair less well as they don’t possess an osmoregulatory organ (Boolootian, 1966). At low salinities, urchins gain weight, and the epidermis loses its pigment; prolonged exposure is fatal. The coelomic fluid of Echinus esculentus is isotonic with seawater (Stickle & Diehl 1987). Because of this, a decrease in salinity within the benchmark may result in lowering the grazing pressure on the biotope and, may in the short-term be beneficial to the biotope.

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 population, although its 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, so that the biotope may come to resemble IR.LIR.KVS.SlatPhyVS or IR.LIR.KVS.SlatPsaVS.  At the benchmark level, IR.LIR.K.Slat.Ft and IR.LIR.K.Slat.P are considered to have ‘High’ resilience 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

The key characterizing species of this biotope, Saccharina latissima is unlikely to be directly affected by this pressure at the prescribed benchmark. Increased competition from other species (such as Laminaria digitata and Laminaria hyperborea) 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 leads 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.

Larval dispersal is in part governed by the local hydrodynamic regime; increased turbulence is associated with an increase in biotope connectivity and therefore a loss of larvae from the local system. A decrease in wave and current mediated water flow is identified by lower connectivity with other sites and a higher settlement rate within the local biotope (Robins et al., 2013).  Therefore an increase in water flow could result in larval loss from the local biotope, which if not balanced by a larval influx from another geographically different population, could result in the demise of the local biotope’s health; with a shift in the age structure of the population and a death of young alga.

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 equally 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. Water movement is a key defining feature of this biotope as Saccharina latissima is characteristic of sheltered, low energy habitats. However, it also occurs in strong water flow where scour (e.g from mobile coarse sediment) and/or turbidity exclude other less opportunistic kelp species (e.g. Laminaria digitata).  Therefore, while mobile sediments (e.g. cobbles) and siltation remain, an increase in water flow of 0.1-0.2 m/s may not have a significant effect on the biotope. Therefore, a ‘High’ resistance and by default a ‘High’ resilience to this pressure is recorded at the benchmark level. Hence, this biotope is regarded as ‘Not sensitive’. 

Emergence regime changes

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

Evidence

The IR.LIR.K.Slat.Ft biotope is predominantly infralittoral while IR.LIR.K.Slat.Pk occurs below 5 m.  Therefore, a change in emergence (as defined by the benchmark) is unlikely to be relevant to IR.LIR.K.Slat.Pk.

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

Both IR.LIR.K.Slat.Ft was recorded from very wave sheltered to extremely sheltered conditions, while IR.LIR.K.Slat.Pk was recorded from sheltered to very sheltered condition (Connor et al., 2004). 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 a 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).  Urchins have been noted to migrate out of kelp biotopes during storms and periods of high wave action, it is suggested that this is done to avoid damage by algal whiplash, which increases in turbulent conditions, temporarily decreasing the grazing pressures on the biotope (Lauzon-Gauy, 2007).  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, 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. The 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 et al. (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.

Sensitivity assessment. The plastic nature of Saccharina latissima’s structure means that it can withstand an increase in wave exposure. However, it may not be able to out-compete other species including Laminaria digitata in more wave exposed conditions, so that the biotope is likely to change, to either mixed kelp biotopes or biotopes dominated by Laminaria digitata in shallow examples or Laminaria hyperborea in more exposed examples, so that the biotope will be lost. Nevertheless, a change in significant wave height of 3-5% is unlikely to have a significant effect on the biotope. Hence a resistance of 'High' is recorded, with a resilience of 'High',  and the biotope is assessed as 'Not sensitive' at the benchmark level.

Transition elements & organo-metal contamination

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

Evidence

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

Hydrocarbon & PAH contamination

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

Evidence

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

Synthetic compound contamination

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

Evidence

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

Radionuclide contamination

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

Evidence

No evidence

Introduction of other substances

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

Evidence

This pressure is Not assessed.

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 was found in the literature, but reduced oxygen concentrations have been shown to inhibit both photosynthesis and respiration in macroalgae (Kinne, 1977). Despite this, macroalgae are thought to buffer the environmental conditions of low oxygen, thereby acting as a refuge for organisms in oxygen depleted regions, especially if the oxygen depletion is short-term (Frieder et al., 2012).  A rapid recovery from a state of low oxygen is expected if the environmental conditions are transient. In addition, this biotope occurs in areas of low water movement, implying that a degree of hypoxia may be inherent in the system.  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).

Grazing of this biotope may be reduced as deoxygenation above the benchmark (anoxia) has been recorded as inducing the death for fish and invertebrates, including Echinus esculentus as a result of a Gyrodinium aureolum phytoplankton bloom in Mounts Bay, Penzance in 1978 (Griffiths et al., 1979).

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. Therefore, based on Saccharina latissima a resistance of ‘High’ is recorded.  Hence resilience is likely to be ‘High’, and the biotope 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).

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 increased the levels of organic matter in their local vicinity.  Evidence from the experimental culture of Saccharina latissima around fish farms showed enhanced growth rates by up to 61% at certain times in the year (Sanderson et al., 2012).  The quality of the nutrient source is also important with depressed growth rates associated with Saccharina latissima growing near a sewage sludge dumping ground in Liverpool Bay, Irish Sea (Burrows, 1971). 

Sea urchins may survive on barren grounds near sewage outfall, anecdotally surviving on dissolved organic material, detritus, plankton and microalgae for prolonged periods (13 years). However the lifespan of the sea urchins in these conditions are severely depressed (Lawrence, 1975). This species may be more resistant to the pressure than Saccharina latissima and may overgraze the biotope, resulting in the loss of the biotope.

Sensitivity assessment. At the benchmark level (a deposit of 100gC/m²/yr) this biotope should be resistant to the pressure, as suggested by the survival and enhanced growth of Saccharina latissima near fish farms where there were high levels of organic matter deposited. 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

A change in substratum type from bedrock to sediment would render the habitat unsuitable because kelp requires a stable substratum on which to settle. No evidence of this biotope occurring on sedimentary substratum was found in the literature. This biotope is anecdotally scarce on the south-east coast of Ireland, in particular, Counties Wicklow and Wexford, due to lack of hard substrata.

Sensitivity assessment.  This biotope is considered to have a resistance of 'None' to this pressure. Resilience is 'Very low' as the pressures is a permanent change so that sensitivity is assessed as ‘High’.

Physical change (to another sediment type)

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

Evidence

'Not relevant' on hard bedrock habitats.

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 occur 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). Echinus esculentus suffer from abrasion via impact from scallop dredges (Bradshaw et al., 2000; Hall-Spencer & Moore, 2000a).  While adults may be able to repair some of their test, most impacts result in the death of the organism. Physical abrasion in this biotope is, therefore, likely to decrease grazing on the kelps and may change the identity of the biotope.

Sensitivity assessment. There is little evidence of 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. Nevertheless, the community is dominated by robust or rapid colonizing species so that resilience is probably 'High' and hence sensitivity '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. 

Echinus esculentus has been recorded in suspended material up to 5-6 mg/l (Comely & Ansell, 1988). Ingestion of sediment by this species has been documented, possibly to extract microalgae (Comely & Ansell, 1988). It is unknown to what extent changes to the turbidity at the benchmark level will affect Echinus esculentus.  The ability of this species to move away from unfavourable conditions suggests that a decrease in grazing could result from a change in turbidity from intermediate to medium turbidity.  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.  However, the biotope is dominated by silt and scour tolerant and/or rapid colonizing 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 other kelp species (e.g. Laminaria digitata)  to increase in abundance 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 spp. 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 would be significantly decreased.  Therefore, the deeper IR.LIR.K.Slat.Pk may be lost, and the depth range of IR.LIR.K.Slat.Ft significantly reduced, and/or replaced by IR.LIR.K.Slat.Pk. Resistance to decreased and increased turbidity is therefore considered 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, in 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).

Smothering of the whole sporophytes is unlikely to last for long, if deposition is light (<5 cm) silt is likely to fall from the fronds to the substratum, especially 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, this is a naturally silty biotope, the organisms should be resistant to this pressure. Epifauna (e.g. ascidians) were reported from vertical surfaces within the biotope, and so are less likely to be smothered (Conner et al., 2004), while the community is depaurate relative to other kelp biotopes because of the siltation and scour.

Sensitivity assessment. Where smothering is short-term (less than 7 days), then this biotope should be relatively resistant. As 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.  However, as the biotope is typical of silted conditions it is probably resistant of short-term deposition of 5 cm sediment. Therefore, 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).

Smothering of the whole sporophytes is unlikely to last for long, if deposition is light (<5 cm) silt is likely to fall from the fronds to the substratum, especially 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, this is a naturally silty biotope, the organisms should be resistant to this pressure. Epifauna (e.g. ascidians) were reported from vertical surfaces within the biotope, and so are less likely to be smothered (Conner et al., 2004), while the community is depaurate relative to other kelp biotopes because of the siltation and scour.

Sensitivity assessment. Where smothering is short-term (less than 7 days), then this biotope should be relatively resistant. The majority of studies have been done in the laboratory; as a result, their results may not be wholly relevant to the reaction of Saccharina latissima to the pressure. As this biotope is recorded from low energy habitats (wave sheltered and weak tidal streams) a deposit of 30 cm of sediment may remain for some time, depending on the local conditions and topography. Such 'Heavy' smothering would probably cover most of the epiflora and epifauna in the biotope (except some on vertical surfaces) and would probably result in death or a significant proportion of the resident species populations, including Saccharina latissima. Therefore, the resistance is probably 'Low'. However, as the resilience is probably 'High', sensitivity is 'Low', 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 alga 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 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). 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 Saccharina latissima so that the IR.LIR.K.Slat.Ft and IR.LIR.K.Slat.Pk may extend to greater depths. 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. 

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 are most relevant to mobile species. Intertidal habitat may be damaged due to the 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 the key characterizing 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 this species, 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).

Sensitivity assessment. No direct evidence was found that might indicate the effects of this pressure on the biotope.

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. In Nova Scotia, Codium fragile competes successfully with native kelps for space including Laminaria digitata, exploiting gaps within the kelp beds. Once established the algal mat created by Codium fragile prevents re-colonization by other macro-algae (Scheibling & 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 was undetermined; their presence illustrated 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 recolonization and recovery of Saccharina latissima beds in the Skagerrak area (Andersen et al., 2011). If an invasion of ephemeral turf algae is coupled with a large-scale disturbance event (e.g. a storm) Saccharina latissima is likely to be vulnerable, and consequently, the whole biotope could be at risk (O’Brien et al., 2015).

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

Sargassum muticum was shown to replace and out-compete leathery, canopy-forming macroalgae such as Saccharina latissima, Halidrys siliquosa, and Fucus spp. and, to a lesser degree, understorey species such as Codium fragile, Chondrus crispus and Dictyota dichotoma in Limfjorden, Denmark between 1984 and 1997 (Staehr et al., 2000; Engelen et al., 2015; de Bettignies et al., 2021).  The invasion in Limfjorden had stabilized by 2005 although many of the native macroalgal species continued to decline (Engelen et al., 2015).  In Limfjorden, the distribution of Sargassum muticum was limited to areas with hard substratum, in particular stones > 10 cm in diameter, while smaller stones, gravel and sand were unsuitable.  It was most abundant between 1 and 4 m in depth but had low cover at 0-0.5 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 one 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).  

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 became a major fouling plant on pontoons (Minchin & Nunn, 2014). Although initially restricted to artificial habitats, such as marinas and ports, it is now widespread in natural habitats in several areas, including Plymouth Sound.

Undaria pinnatifida seems to settle better on artificial substrata (e.g. floats, marinas or piers) than on natural rocky shores among local kelps (Vaz-Pinto et al., 2014). It is found predominantly in low intertidal to shallow subtidal habitats (Epstein et al., 2019b) and is significantly more abundant on artificial substrata compared to natural rocky substrata (Heiser et al., 2014; Epstein & Smale, 2018). James (2017) suggested that Undaria pinnatifida could out-compete native species on artificial substrata (such as marinas and wharf structures). 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 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 is 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. 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.

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 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 both Sargassum muticum and Undaria pinnatifida can both compete with and co-exist with Saccharina latissima, depending on local conditions. This Saccharina latissima dominated biotope (IR.LIR.K.Slat.Pk) occurs in low energy, silty environments with a full or variable salinity, which are the preferred habitat conditions for Sargassum muticum and Undaria pinnatifida.  The dense canopy of Saccharina latissima may inhibit colonization but any disturbance may allow Sargassum and/or Undaria to colonize. However, Undaria pinnatifida is recorded from 0-10 m in depth (OBIS, 2022), while Epstein et al. (2019b) suggest that its depth range is +1 m to -4 m, and it is only likely to be a threat to the shallow examples of the biotope. Sargassum muticum also prefers wave sheltered shallow sites in the sublittoral fringe and shallow infralittoral.  It was reported to out-compete and replace Saccharina latissima in the turbid waters of the Limfjorden, and achieve maximum abundance at 1-4 m (Staehr et al., 2000; Engelen et al., 2015).  But Strong & Dring (2011) concluded that Sargassum was not a threat to Saccharina latissima in the Dorn, Strangford Lough where it coexisted and grew better in mixed stands. Therefore, competition with Sargassum is probably site-specific and dependent on local conditions.  

Sargassum may colonize the biotope at low abundance but it is light-limited and restricted to the shallow infralittoral or sublittoral fringe and, therefore, unlikely to out-compete Saccharina lattissima at the depths typical of this biotope. However, Undaria pinnatifida may be able to colonize this biotope and then either co-exist with or out-compete Saccharina latissima, resulting in a potentially significant (25-75%) reduction in the abundance or extent of the native kelp.  Undaria pinnatifida is recorded from 0-10 m in depth (OBIS, 2022), while Epstein et al. (2019b) suggest that its depth range is +1 m to -4 m, and it is only likely to be a threat to the shallow examples of the biotope (that is 0-10 m). Therefore, resistance is assessed as ‘Low’ for shallow examples of the biotope, i.e. above 10 m in depth, while it is probably ‘Not relevant’ to deeper examples (>10 m). Recovery after invasion by Sargassum or Undaria, although rapid, would require direct intervention (removal) so that resilience is assessed as ‘Very low’. Hence, the sensitivity of shallow examples of the biotope 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, Sargassum muticum and Undaria pinnatifida.

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 two algal pathogens, Pseudoalteromonas elyakovii and Algicola bacteriolytica. Pseudomonads produce antibiotics which prevent Saccharina latissima’s infection, suggesting that this biotope’s resistance to disease is population and location specific (Nagel et al., 2012).

There is no evidence in the literature that infection by microbial pathogens results in the mass death of kelp populations and the kelp themselves are known to regulate bacterial infections through iodine metabolism (Cosse et al., 2009).  Based on the lack of reported mortalities of the characterizing and associated species, the resistance is assessed as ‘High’ resistance to this pressure. Hence, resilience is assessed as ‘High’ and the biotope is assessed as ‘Not sensitive’. 

Removal of target species

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

Evidence

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 the 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 the 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 the UK and Irish waters, resulting in habitats dominated by invertebrates and commercially undesirable fish such as the lesser spotted cat shark (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. The deforestation by urchins is restricted and patchy (although some have been noted in Scotland; Smale et al., 2013) but could be a result of this shift, leading to a temporally more stable, less dynamic biotope.

Sensitivity assessment. Due to the methods of harvesting used for Saccharina latissima, with the emphasis on aquaculture rather than wild harvesting, little evidence for the resilience of this biotope to harvesting exists. It can be presumed however that 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. Nevertheless, resilience is probably ‘High’, so that 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.  In healthy macroalgae communities, many species contribute to the balanced condition of the ecosystem. Disrupting this balance may cause top-down consequences for the biotope; for example, overfishing of top predators in Norwegian waters was thought to have resulted in an urchin bloom, subsequent overgrazing and proliferation of urchin barrens (Steneck et al., 2004).

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