Alaria esculenta, Mytilus edulis and coralline crusts on very exposed sublittoral fringe bedrock

Summary

UK and Ireland classification

Description

Very exposed sublittoral fringe bedrock characterized by the kelp Alaria esculenta and dense patches of small Mytilus edulis, both of which grow over a dense cover of encrusting coralline algae. Foliose red algae may also be present, but the species composition and their abundance varies between sites. Species such as Corallina officinalis, Mastocarpus stellatus and Plocamium cartilagineum occur widely. Limpets and barnacles are often common. Patches of anemones (such as Cylista elegans) and the hydroid Tubularia indivisa also occur in wave-surged areas. Laminaria digitata is usually absent, although stunted plants may be present at a few sites (typically greater than frequent). On very exposed shores this biotope is usually found beneath the Mytilus edulis-barnacle zone (ELR.MytB) and above the sublittoral Laminaria hyperborea forest (EIR.LhypR or EIR.LhypFa). In extremely exposed areas the Alaria zone may extend as deep at 15 m, where it generally has less Mytilus and greater densities of Tubularia (e.g. Barra and shallow areas of Rockall). This biotope is, however, distinguished from the deep Alaria forest (EIR.AlaAnSC) found on Rockall by its lack of short turf-forming hydroids. On less exposed shores an Alaria-dominated zone may, however, lie immediately above a narrow Laminaria digitata zone (MIR.Ldig). This biotope can also occur on exposed steep or vertical shores, where wave-crash restricts the growth of Laminaria digitata (JNCC, 2015, 2022).

Depth range

Lower shore, 0-5 m

Additional information

-

Listed By

Sensitivity reviewHow is sensitivity assessed?

Sensitivity characteristics of the habitat and relevant characteristic species

IR.HIR.KFaR.Ala and IR.HIR.KFaR.AlaAnCrSp (plus associated sub-biotopes) are characterized by the northern/boreal kelp Alaria esculenta and are indicative of very wave exposed sublittoral bedrock. IR.HIR.KFaR.Ala occurs predominantly on sublittoral fringe bedrock to a depth of 1-2 m. However, at extremely exposed sites wave action can prevent competition from Laminaria hyperborea in the infralittoral zone and the Alaria esculenta defined biotopes IR.HIR.KFaR.Ala.Myt and IR.HIR.KFaR.AlaAnCrSp can extend to a depth of 15-35 m. In slightly less wave exposed conditions Laminaria digitata can compete with Alaria esculenta and in the sub-biotope; IR.HIR.KFaR.Ala.Ldig, the two species form a mixed canopy.

The understorey community beneath Alaria esculenta canopies is defined by the degree of wave exposure at the site.  Common understorey species across Alaria esculenta biotopes are encrusting coralline algae and Corallina officinalis turf. IR.HIR.KFaR.AlaAnCrSp has only been recorded on steep/vertical bedrock at Rockall, Scotland. Extreme wave exposure at Rockall excludes Laminaria hyperborea and IR.HIR.KFaR.AlaAnCrSp extends from 14-35 m, and the rock surface is covered by a dense turf of anthozoans such as Cylista elegans, Phellia gausapata and Corynactis viridis, encrusting sponges and coralline algae.  In the sub-biotope IR.HIR.KFaR.Ala.Myt, Mytillus edulis is an abundant component of the understorey, while patches of anthozoans and the hydroid Tubularia spp. occur in more wave-surged areas.  In the mixed Alaria esculenta & Laminaria digitata biotope IR.HIR.KFaR.Ala.Ldig, the red seaweeds; Palmaria palmata, Mastocarpus stellatus and Chondrus crispus are predominant features of the understorey.

In undertaking this assessment of sensitivity, an account is taken of knowledge of the biology of all characterizing species/taxa in the biotope. In this sensitivity assessment, Alaria esculenta is the primary focus of research, as in the dominant characteristic species, without which the biotope would not be recognized.  However, Laminaria digitata, plus understorey species Corallina officinalis, encrusting algae, Mytilus edulis and red seaweeds also define IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus their associated sub-biotopes. Examples of important species groups are mentioned where appropriate.

Resilience and recovery rates of habitat

Alaria esculenta is a perennial kelp found in the North Atlantic (Birkett et al., 1998b) which dominates the sublittoral fringe in areas exposed to severe wave action or where water surges along the sides of gullies or steep/vertical bedrock (Lewis, 1964; Connor et al.,2004). In extreme wave action Laminaria digitata and Laminaria hyperborea are likely to become damaged and die back, whereas morphological features and high growth rates allow Alaria esculenta to survive in such conditions (Birkett et al., 1998). Alaria esculenta has a compact holdfast, a flexible “short” stipe and a flexible frond with a conspicuous reinforcing midrib (Birkett et al., 1998b). Maximum growth rates are recorded in April-May which can exceed 20 cm/month (Birkett et al., 1998b). From June-July growth rates slow and continual erosion along the frond margins can reduce the sporophyte to a holdfast, stipe and short length of blade, in which state the sporophyte overwinters. In extremely wave exposed conditions, especially in winter months, the blade may be reduced to just the midrib. The sporophyte can reach a total length of 4 m (Werner & Kraan, 2004), fronds can reach a total length of 2 m, however, growth rates are locally variable and are more typically 30-90cm in length (Birkett et al., 1998b). Alaria esculenta can reach maturity rapidly in 10-14 months and lives for 4-7 years (Birkett et al., 1998b; Baardseth, 1956).

Alaria esculenta has a heteromorphic life history (Fredersdorf et al., 2009). Between November to March a vast number of meiotic haploid zoospores are released from sori located on sporophylls (found at the top of the stipe).  Zoospore dispersal is greatly influenced by local water movements and zoospore densities. Laminarian spores also need to settle in high density so that the resultant gametophytes are close enough to cross-fertilize (Fredriksen et al., 1995). Recruitment of Alaria escuolenta may, therefore, be influenced by the proximity of mature sporophytes producing viable zoospores (Kain, 1979; Fredriksen et al., 1995). Laminarians are expected to disperse zoospores over considerable distances. However, Alaria esculenta may have a lower dispersal capacity than other Laminarins due to the basal location of the sporophylls Norton (1992). Sundene (1962) agreed with Norton (1992) in an Alaria esculenta translocation experiment conducted in a Norwegian fjord, observing that Alaria esculenta germlings were restricted to within 10m of the parental source.

Alaria esculenta is an opportunistic colonizing species (Kain 1975a; Hawkins & Harkin 1985; Hill, 1993; Engelen, 2010). Alaria esculenta can settle on bare surfaces, including mobile boulders and in deeper water than the infralittoral fringe Alaria esculenta often appears early in the algal succession (ca 3 months after clearance of dominant algae) before being outcompeted by other kelp species (in moderately wave exposed shores). During kelp canopy removal experiments in the Isle of Man, Hawkins & Harkin (1985) found that in moderately wave exposed areas cleared of Laminaria digitata (the dominant canopy forming species). Alaria esculenta became the dominant canopy algae within 9 months (October - June) and Laminaria digitata did not re-establish dominance within the study period (15 months). In areas of moderate to sheltered wave exposure Alaria esculenta colonized the blocks within 1 month of clearance and reached 25% coverage within 5 months but within 7 months Laminaria digitata had out-competed Alaria esculenta and re-established dominance within the community reaching ~90-95% coverage.  Kain (1975a) conducted a similar experiment to Hawkins & Harkin (1985), however over a longer time period (>2 year).  

Blue mussels, Mytilus edulis, are sessile, attached organisms that are unable to repair significant damage to individuals. Mussels do not reproduce asexually and, therefore, the only mechanism for recovery from significant impacts (where resistance is assessed as ‘None’, ‘Low’ or ‘Medium’) is larval recruitment to the bed or the area where previously a bed existed. Spawning occurs in spring and later summer allowing two periods of recruitment (Seed, 1969).  Mytilus edulis has a high fecundity producing >1,000,000 eggs per spawning event.  Larvae stay in the plankton for between 20 days to two months depending on water temperature (Bayne, 1976).  In unfavourable conditions, they may delay metamorphosis for 6 months (Lane et al., 1985).  Larval dispersal depends on the currents and the length of time they spend in the plankton.  Larvae subject to ocean currents for up to six months can have a high dispersal potential. Settlement occurs in two phases, an initial attachment using their foot (the pediveliger stage) and then a second attachment by the byssus thread before which they may alter their location to a more favourable one (Bayne, 1964).  The final settlement often occurs around or between individual mussels of an established population. In areas of high water flow the mussel bed will rely on recruitment from other populations as larvae will be swept away and therefore recovery will depend on recruitment from elsewhere. 

Mainwaring et al. (2014) reviewed the evidence for recovery of Mytilus.edulis beds from disturbance and an earlier study by Seed & Suchanek (1992) reviewed studies on the recovery of ‘gaps’ in Mytilus spp. beds.  It was concluded that beds occurring high on the shore and on less exposed sites took longer to recover after a disturbance event than beds found low on the shore or at more exposed sites.  However, the slowest recovering sites (high shore and sheltered shores) are at the least risk of natural disturbance and often considered more ‘stable’ (Lewis, 1964) as they are less vulnerable to removal by wave action or wave driven logs. Continued disturbance will lead to a patchy distribution of mussels.

Recruitment of Mytilus edulis is often sporadic, occurring in unpredictable pulses (Seed & Suchanek, 1992), although persistent mussel beds can be maintained by relatively low levels or episodic recruitment (McGrorty et al., 1990).  A good annual recruitment could result in rapid recovery (Holt et al., 1998).  However, the unpredictable pattern of recruitment based on environmental conditions could result in recruitment taking much longer.  

In some long-term studies of Mytilus californianus it was observed that gaps could continue to increase in size post-disturbance due to wave action and predation (Paine & Levin, 1981; Brosnan & Crumrine, 1994; Smith & Murray, 2005) potentially due to the weakening of the byssus threads leaving them more vulnerable to environmental conditions (Denny 1987).  On rocky shores, barnacles and fucoids are often quick to colonize the ‘gaps’ created.  The presence of macroalgae appears to inhibit recovery whilst the presence of barnacles enhances subsequent mussel recruitment (Seed & Suchanek 1992). Brosnan & Crumrine (1994) observed little recovery of the congener Mytilus californianus in two years after trampling disturbance.  Paine & Levin (1981) estimated that recovery times of beds could be between 8-24 years while Seed & Suchaneck (1992) suggested it could take longer-time scales, suggesting that meaningful recovery is unlikely in some areas.  It has, however, been suggested that Mytilus edulis recovers quicker than other Mytilus species (Seed & Suchanek 1992), which may mean that these predicted recovery rates are too low for Mytilus edulis.

Corallina officinalis produces spores over a protracted period and can colonize artificial substratum within one week in the intertidal (Harlin & Lindbergh, 1977; Littler & Kauker, 1984). The crustose base enables Corallina officinalis to survive extreme wave exposure and damage (loss of fronds), and to take advantage (colonize) of space left after winter storms have removed competing macroalgae (Littler & Kauker, 1984). The mobile interstitial fauna of the coralline turf is reduced by trampling (Brown & Taylor, 1999) but is likely to recruit to or recolonize the turf from the surrounding communities. Encrusting and erect corallines are also known to stimulate the settlement of a variety of marine invertebrate larvae and algal spores. Corallina officinalis is capable of colonizing new substratum rapidly. In experimental plots, 15 percent cover of fronds returned within 3 months (Littler & Kauker, 1985) and Brown & Taylor (1999) noted that the articulated coralline algal turf community on a New Zealand shore returned to normal levels within 3 months of trampling events, although they suggested that a return to its previous cover may take longer.

Resilience assessment. Alaria esculenta is an opportunistic and rapidly colonizing species (see above) capable of growing 20 cm/month in optimal conditions, reaching maturity within 10-14 months, and often appearing early in the algal succession (c. 3 months after clearance of dominant algae). In canopy removal experiments in the Isle of Man, Hawkins & Harkin (1985) found that areas cleared of Laminaria digitata (moderately exposed) Alaria esculenta became the dominant canopy algae within 9 months (October - June). Recovery rates of Mytilus edulis beds from different levels of impact is very limited and whether these rates are similar, or not, between biotopes is largely unclear.  Recovery rates are clearly determined by a range of factors such as the degree of impact, the season of impact, larval supply and local environmental factors including hydrodynamics so that confidence in the applicability of generic assessments is ‘Low’. Overall, Mytilus spp. populations are considered to have a strong ability to recover from environmental disturbance (Holt et al., 1998; Seed & Suchaneck, 1992).  A good annual recruitment may allow a bed to recovery rapidly, though this cannot always be guaranteed within a certain time-scale due to the episodic nature of Mytilus edulis recruitment (Lutz & Kennish, 1992; Seed & Suchanek, 1992) and the influence of site-specific variables. Corallina officinalis is capable of colonizing new substratum rapidly. In experimental plots, 15 percent cover of fronds returned within three months (Littler & Kauker, 1985) and Brown & Taylor (1999) noted that the articulated coralline algal turf community on a New Zealand shore returned to normal levels within three months of trampling events, although they suggested that a return to its previous cover may take longer. 

Therefore, the resilience of IR.HIR.KFaR.Ala.Myt biotopes has been assessed as High. An exception is made for permanent or ongoing (long-term) pressures where recovery is not possible as the pressure is irreversible, in which case resilience is assessed as ‘Very low’ by default.  

The resilience and the ability to recover from human induced pressures is a combination of the environmental conditions of the site, the frequency (repeated disturbances versus a one-off event) and the intensity of the disturbance.  Recovery of impacted populations will always be mediated by stochastic events and processes acting over different scales including, but not limited to, local habitat conditions, further impacts and processes such as larval supply and recruitment between populations. Full recovery is defined as the return to the state of the habitat that existed prior to impact.  This does not necessarily mean that every component species has returned to its prior condition, abundance or extent but that the relevant functional components are present, and the habitat is structurally and functionally recognizable as the initial habitat of interest. It should be noted that the recovery rates are only indicative of the recovery potential.

Climate Change Pressures

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ResistanceResilienceSensitivity
Global warming (extreme) [Show more]

Global warming (extreme)

Extreme emission scenario (by the end of this century 2081-2100) benchmark of:

  • A 5°C rise in SST and NBT (coastal to the shelf seas),

  • A 6°C rise in surface air temperature (in eulittoral and supralittoral habitats).

  • A 1°C rise in Deep-sea habitats (>200 m) off the continental shelf, and

  • A 5°C rise in surface air temperature in intertidal habitats exclusive to Scotland. Further detail.

Evidence

The distribution of kelp is strongly influenced by climatic conditions; therefore, kelp species are extremely sensitive to the ongoing ocean warming (Kain, 1979; Van Den Hoek, 1982; Breeman, 1990; Lüning, 1990; Assis et al., 2016; Smale, 2020). Northern distribution boundaries are set by winter temperatures that are lethal, or summer temperatures too low for growth and/or reproduction, whilst southern limits are set by high lethal summer temperatures or winter temperatures too high for induction of a crucial step in the life cycle (Breeman, 1990). Kelps have a high dependence on ocean temperatures, which make them highly vulnerable to ocean warming (Assis et al., 2014). As temperatures increase, populations found towards the upper limit of their temperature range may be adversely affected by warming as physiological thresholds are exceeded (Wiens, 2016). Thermal stress can lead to mortality and consequent population-level effects, such as decreased abundance, altered size structure, local extinction and range contractions (Smale, 2020). 

Alaria esculenta is a polar to cold-temperate species that has been recorded from Brittany, France to Northern Norway (Birkett et al., 1998b). Sea temperature regulates metabolism and reproduction and defines the regional distribution of Alaria esculenta (Fredersdorf et al., 2009). The southern limit of Alaria esculenta has been defined at the 20°C isotherm (Munda & Lüning, 1977; Fredersdorf et al., 2009), however, it is more common north of the 16°C isotherm (Munda & Lüning, 1977; Van der Hoek, 1982; Kraan, 2020). As a result of this upper temperature threshold, Alaria esculenta is largely absent from the southern North Sea and the English Channel where summer temperatures exceed 16°C. 

Munda & Lüning (1977) observed temperatures of 16-17°C, sustained over 2 weeks in Helgoland, Germany, were lethal to resident Alaria esculenta. Experimental observations showed acute exposure to ≥21°C is lethal to Alaria esculenta causing bleaching and disintegration (Sundene, 1962; Fredersdorf et al., 2009). At its northern range edge (Svalbard), it is a prominent macroalga on the sublittoral fringe bedrock.  At these northern latitudes, average summer temperature can reach 5°C, with an average annual sea temperature of 3°C (1980-2014, Beszczynska-Möller & Dye, 2013). Experimental observations conducted by Fredersdorf et al. (2009) found the optimal temperature for sporophyte photosynthesis was within the range of 13-17°C, however, the optimal temperature for Alaria esculenta germination was 2-12°C (Fredersdorf et al., 2009).

A study by Zacher et al. (2019) observed gametogenesis and sporophyte formation of Alaria esculenta to be inhibited at 15°C. Zacher et al. (2019) also observed sporophyte growth to be slower at 10°C than at 4°C. Equally, Park et al. (2017) noted Alaria esculenta female gametophytes to produce more sporophytes at 5°C than at 10°C, and with no sporophytes at 15°C. However, Kraan. (2020) reports Alaria esculenta gametophytes to able to survive -1.5 to 20 °C. The literature suggests that the distribution of Alaria esculenta is possibly determined by the temperature requirements for gametogenesis or reproduction rather than the temperature tolerance of the gametophyte or sporophyte (Zacher et al., 2019; Kraan, 2020). 

Mytilus edulis is a eurytopic species found in a wide temperature range from mild, subtropical regions to areas that frequently experience freezing conditions and are vulnerable to ice scour (Seed & Suchanek 1992). In the north Atlantic, this species occurs from Norway to the coast of Spain. In the western Atlantic, Mytilus edulis is reported to be expanding its range pole-wards and has reappeared in Svalbard, due to an increase in sea temperature in that region (Berge et al., 2005). However, its equatorial limits have contracted approximately 350 km north of its previous southern limits in Cape Hatteras, North Carolina, due to increases in water temperature beyond the lethal limit (Jones et al., 2009).

In British waters 29°C was recorded as the upper sustained thermal tolerance limit for Mytilus edulis (Read & Cumming, 1967; Almada-Villela, et al., 1982), although it is thought that European mussels will rarely experience temperatures above 25°C (Seed & Suchanek, 1992). At the upper range of a mussels tolerance limit, heat shock proteins are produced, indicating high stress levels (Jones et al., 2010).  After a single day at 30°C, heat shock proteins were still present over 14 days later, although at a reduced level.  Increased temperatures can also affect reproduction in Mytilus edulis (Myrand et al., 2000).  In shallow lagoons, mortality began in late July at the end of a major spawning event when temperatures peaked at >20°C.  These mussels had a low energetic content post-spawning and had stopped shell growth.  It is likely that the high temperatures caused mortality due to the reduced condition of the mussels post-spawning (Myrand et al., 2000). Similarly, Hiebenthal et al. (2013) found that the growth rate decreased by 60% as temperatures increased from 20 - 25°C and resulted in 25% mortality under experimental conditions. Incze et al. (1980) found that Mytilus edulis growth decreased at 20°C and mortality occurred at 25°C, although mortality occurred at lower temperatures when phytoplankton abundance was low, suggesting that mortality occurred through a combination of reducing food source at a time of metabolic stress.

Rising air temperatures can also lead to significant mortality in Mytilus edulis. Intertidal ecosystems are likely to be more negatively impacted than subtidal ecosystems, due to their increased daily and seasonal variations in temperatures (Jones et al., 2009). Temperature changes may also lead to indirect effects. For example, an increase in temperature increases the mussels’ susceptibility to pathogens (Vibrio tubiashii) in the presence of relatively low concentrations of copper (Parry & Pipe, 2004).  Increased temperatures may also allow for range expansion of parasites or pathogens which will have a negative impact upon the health of the mussels if they become infected. There is evidence that increases in temperature will also give a competitive advantage to invasive species.  For example, in the Dutch Wadden Sea mild winters favour Magallana gigas recruitment while cold winters favour Mytilus edulis (Deiderich, 2005).

Alaria esculenta has already shown signs of contracting its range in the UK as a result of ocean warming (Mieszkowska, 2016). The abundance of Alaria esculenta has declined in shallow subtidal zones around the western English Channel and is predicted to disappear from south-west England and the coasts of western and southern Ireland (Mieszkowska et al., 2005; Birchenough, et al., 2013).

Corallina officinalis may tolerate between -4 to 28°C (Lüning, 1990), although when Colthart & Johansen (1973) exposed this species to a number of different temperatures, they found that growth was maintained at 18°C and ceased at 25°C. Abrupt temperature changes (10°C in California, Seapy & Littler 1984; 4.8 to 8.5°C, Hawkins & Hartnoll, 1985) resulted in dramatic declines. However, in both cases recovery was rapid, suggesting that the crustose bases survived. 

Sensitivity assessment. Alaria esculenta is nearing its southern limits in the UK, with this species only occurring as far south as Brittany, France. Sea surface temperatures (SST) around the UK currently fall between 6-19°C (Huthnance, 2010). The available evidence suggests that the effects of ocean warming may occur throughout the year.  If winter temperatures exceed 12°C this is likely to inhibit germination, whilst summer temperatures greater than 20°C will cause mortality of Alaria esculentaAlaria esculenta is competitively inferior to Laminaria digitata in the northeast Atlantic (Hawkins & Harkin, 1985) where it is confined to more exposed shores and can colonize sheltered environments only if Laminaria digitata is removed. As temperatures rise to up to 20°C, it is expected that the competitive ability of this species will decrease further, while as temperatures rise above 20°C Alaria esculenta will be lost, with more warm adapted algae taking its place. Brodie et al. (2014) predict that Alaria esculenta will be completely lost from Boreal habitats by the end of this century, whilst all kelp species will be lost from the Lusitanian region, replaced by smaller, fleshy algae.

Sea surface temperatures around the UK are currently between 6-19°C (Huthnance, 2010). Under the middle emission scenario Alaria esculenta is likely to be lost from most of the UK, although it may manage to maintain some populations in Scotland, where current summer temperatures often reach 14°C, leading to potential summer temperatures of 17°C. Corallina officinalis, Mytilus edulis and other warm-tolerant species should be able to cope with temperature increases under a middle emission scenario in UK waters. As Alaria esculenta is the main characterizing species for this study and is expected to be lost from a large portion of the UK, under this scenario resistance is assessed as ‘Low’. Resilience is assessed as ‘Very Low’, as loss is likely to be a long-term decline, due to the long-term nature of ocean warming. Therefore, this biotope IR.HIR.KFaR.Ala.Myt is assessed as having ‘High’ sensitivity to ocean warming under a middle emission scenario.

For the high emission scenario and extreme scenario, sea temperatures may rise by 4-5°C to give potential southern summer temperatures of 23-24°C and northern summer temperatures of 18-19°C. Under these scenarios, it is likely that Alaria esculenta will be lost almost completely from the UK. Therefore, resistance is assessed as ‘None’, and resilience is assessed as ‘Very low’. Overall, this biotope Ala.Myt is assessed as having ‘High’ sensitivity to ocean warming for the high emission scenario and the extreme scenario.  

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Global warming (high) [Show more]

Global warming (high)

High emission scenario (by the end of this century 2081-2100) benchmark of:

  • A 4°C rise in SST, NBT (coastal to the shelf seas) and surface air temperature (in eulittoral and supralittoral habitats).

  • A 1°C rise in Deep-sea habitats (>200 m) off the continental shelf, and

  • A 3°C rise in surface air temperature in intertidal habitats exclusive to Scotland. Further detail.

Evidence

The distribution of kelp is strongly influenced by climatic conditions; therefore, kelp species are extremely sensitive to the ongoing ocean warming (Kain, 1979; Van Den Hoek, 1982; Breeman, 1990; Lüning, 1990; Assis et al., 2016; Smale, 2020). Northern distribution boundaries are set by winter temperatures that are lethal, or summer temperatures too low for growth and/or reproduction, whilst southern limits are set by high lethal summer temperatures or winter temperatures too high for induction of a crucial step in the life cycle (Breeman, 1990). Kelps have a high dependence on ocean temperatures, which make them highly vulnerable to ocean warming (Assis et al., 2014). As temperatures increase, populations found towards the upper limit of their temperature range may be adversely affected by warming as physiological thresholds are exceeded (Wiens, 2016). Thermal stress can lead to mortality and consequent population-level effects, such as decreased abundance, altered size structure, local extinction and range contractions (Smale, 2020). 

Alaria esculenta is a polar to cold-temperate species that has been recorded from Brittany, France to Northern Norway (Birkett et al., 1998b). Sea temperature regulates metabolism and reproduction and defines the regional distribution of Alaria esculenta (Fredersdorf et al., 2009). The southern limit of Alaria esculenta has been defined at the 20°C isotherm (Munda & Lüning, 1977; Fredersdorf et al., 2009), however, it is more common north of the 16°C isotherm (Munda & Lüning, 1977; Van der Hoek, 1982; Kraan, 2020). As a result of this upper temperature threshold, Alaria esculenta is largely absent from the southern North Sea and the English Channel where summer temperatures exceed 16°C. 

Munda & Lüning (1977) observed temperatures of 16-17°C, sustained over 2 weeks in Helgoland, Germany, were lethal to resident Alaria esculenta. Experimental observations showed acute exposure to ≥21°C is lethal to Alaria esculenta causing bleaching and disintegration (Sundene, 1962; Fredersdorf et al., 2009). At its northern range edge (Svalbard), it is a prominent macroalga on the sublittoral fringe bedrock.  At these northern latitudes, average summer temperature can reach 5°C, with an average annual sea temperature of 3°C (1980-2014, Beszczynska-Möller & Dye, 2013). Experimental observations conducted by Fredersdorf et al. (2009) found the optimal temperature for sporophyte photosynthesis was within the range of 13-17°C, however, the optimal temperature for Alaria esculenta germination was 2-12°C (Fredersdorf et al., 2009).

A study by Zacher et al. (2019) observed gametogenesis and sporophyte formation of Alaria esculenta to be inhibited at 15°C. Zacher et al. (2019) also observed sporophyte growth to be slower at 10°C than at 4°C. Equally, Park et al. (2017) noted Alaria esculenta female gametophytes to produce more sporophytes at 5°C than at 10°C, and with no sporophytes at 15°C. However, Kraan. (2020) reports Alaria esculenta gametophytes to able to survive -1.5 to 20 °C. The literature suggests that the distribution of Alaria esculenta is possibly determined by the temperature requirements for gametogenesis or reproduction rather than the temperature tolerance of the gametophyte or sporophyte (Zacher et al., 2019; Kraan, 2020). 

Mytilus edulis is a eurytopic species found in a wide temperature range from mild, subtropical regions to areas that frequently experience freezing conditions and are vulnerable to ice scour (Seed & Suchanek 1992). In the north Atlantic, this species occurs from Norway to the coast of Spain. In the western Atlantic, Mytilus edulis is reported to be expanding its range pole-wards and has reappeared in Svalbard, due to an increase in sea temperature in that region (Berge et al., 2005). However, its equatorial limits have contracted approximately 350 km north of its previous southern limits in Cape Hatteras, North Carolina, due to increases in water temperature beyond the lethal limit (Jones et al., 2009).

In British waters 29°C was recorded as the upper sustained thermal tolerance limit for Mytilus edulis (Read & Cumming, 1967; Almada-Villela, et al., 1982), although it is thought that European mussels will rarely experience temperatures above 25°C (Seed & Suchanek, 1992). At the upper range of a mussels tolerance limit, heat shock proteins are produced, indicating high stress levels (Jones et al., 2010).  After a single day at 30°C, heat shock proteins were still present over 14 days later, although at a reduced level.  Increased temperatures can also affect reproduction in Mytilus edulis (Myrand et al., 2000).  In shallow lagoons, mortality began in late July at the end of a major spawning event when temperatures peaked at >20°C.  These mussels had a low energetic content post-spawning and had stopped shell growth.  It is likely that the high temperatures caused mortality due to the reduced condition of the mussels post-spawning (Myrand et al., 2000). Similarly, Hiebenthal et al. (2013) found that the growth rate decreased by 60% as temperatures increased from 20 - 25°C and resulted in 25% mortality under experimental conditions. Incze et al. (1980) found that Mytilus edulis growth decreased at 20°C and mortality occurred at 25°C, although mortality occurred at lower temperatures when phytoplankton abundance was low, suggesting that mortality occurred through a combination of reducing food source at a time of metabolic stress.

Rising air temperatures can also lead to significant mortality in Mytilus edulis. Intertidal ecosystems are likely to be more negatively impacted than subtidal ecosystems, due to their increased daily and seasonal variations in temperatures (Jones et al., 2009). Temperature changes may also lead to indirect effects. For example, an increase in temperature increases the mussels’ susceptibility to pathogens (Vibrio tubiashii) in the presence of relatively low concentrations of copper (Parry & Pipe, 2004).  Increased temperatures may also allow for range expansion of parasites or pathogens which will have a negative impact upon the health of the mussels if they become infected. There is evidence that increases in temperature will also give a competitive advantage to invasive species.  For example, in the Dutch Wadden Sea mild winters favour Magallana gigas recruitment while cold winters favour Mytilus edulis (Deiderich, 2005).

Alaria esculenta has already shown signs of contracting its range in the UK as a result of ocean warming (Mieszkowska, 2016). The abundance of Alaria esculenta has declined in shallow subtidal zones around the western English Channel and is predicted to disappear from south-west England and the coasts of western and southern Ireland (Mieszkowska et al., 2005; Birchenough, et al., 2013).

Corallina officinalis may tolerate between -4 to 28°C (Lüning, 1990), although when Colthart & Johansen (1973) exposed this species to a number of different temperatures, they found that growth was maintained at 18°C and ceased at 25°C. Abrupt temperature changes (10°C in California, Seapy & Littler 1984; 4.8 to 8.5°C, Hawkins & Hartnoll, 1985) resulted in dramatic declines. However, in both cases recovery was rapid, suggesting that the crustose bases survived. 

Sensitivity assessment. Alaria esculenta is nearing its southern limits in the UK, with this species only occurring as far south as Brittany, France. Sea surface temperatures (SST) around the UK currently fall between 6-19°C (Huthnance, 2010). The available evidence suggests that the effects of ocean warming may occur throughout the year.  If winter temperatures exceed 12°C this is likely to inhibit germination, whilst summer temperatures greater than 20°C will cause mortality of Alaria esculentaAlaria esculenta is competitively inferior to Laminaria digitata in the northeast Atlantic (Hawkins & Harkin, 1985) where it is confined to more exposed shores and can colonize sheltered environments only if Laminaria digitata is removed. As temperatures rise to up to 20°C, it is expected that the competitive ability of this species will decrease further, while as temperatures rise above 20°C Alaria esculenta will be lost, with more warm adapted algae taking its place. Brodie et al. (2014) predict that Alaria esculenta will be completely lost from Boreal habitats by the end of this century, whilst all kelp species will be lost from the Lusitanian region, replaced by smaller, fleshy algae.

Sea surface temperatures around the UK are currently between 6-19°C (Huthnance, 2010). Under the middle emission scenario Alaria esculenta is likely to be lost from most of the UK, although it may manage to maintain some populations in Scotland, where current summer temperatures often reach 14°C, leading to potential summer temperatures of 17°C. Corallina officinalis, Mytilus edulis and other warm-tolerant species should be able to cope with temperature increases under a middle emission scenario in UK waters. As Alaria esculenta is the main characterizing species for this study and is expected to be lost from a large portion of the UK, under this scenario resistance is assessed as ‘Low’. Resilience is assessed as ‘Very Low’, as loss is likely to be a long-term decline, due to the long-term nature of ocean warming. Therefore, this biotope IR.HIR.KFaR.Ala.Myt is assessed as having ‘High’ sensitivity to ocean warming under a middle emission scenario.

For the high emission scenario and extreme scenario, sea temperatures may rise by 4-5°C to give potential southern summer temperatures of 23-24°C and northern summer temperatures of 18-19°C. Under these scenarios, it is likely that Alaria esculenta will be lost almost completely from the UK. Therefore, resistance is assessed as ‘None’, and resilience is assessed as ‘Very low’. Overall, this biotope Ala.Myt is assessed as having ‘High’ sensitivity to ocean warming for the high emission scenario and the extreme scenario.  

None
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Very Low
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High
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Global warming (middle) [Show more]

Global warming (middle)

Middle emission scenario (by the end of this century 2081-2100) benchmark of:

  • A 3°C rise in SST, NBT (coastal to the shelf seas) and surface air temperature (in eulittoral and supralittoral habitats).

  • A 1°C rise in Deep-sea habitats (>200 m) off the continental shelf.

  • A 2°C rise in surface air temperature in intertidal habitats exclusive to Scotland. Further detail.

Evidence

The distribution of kelp is strongly influenced by climatic conditions; therefore, kelp species are extremely sensitive to the ongoing ocean warming (Kain, 1979; Van Den Hoek, 1982; Breeman, 1990; Lüning, 1990; Assis et al., 2016; Smale, 2020). Northern distribution boundaries are set by winter temperatures that are lethal, or summer temperatures too low for growth and/or reproduction, whilst southern limits are set by high lethal summer temperatures or winter temperatures too high for induction of a crucial step in the life cycle (Breeman, 1990). Kelps have a high dependence on ocean temperatures, which make them highly vulnerable to ocean warming (Assis et al., 2014). As temperatures increase, populations found towards the upper limit of their temperature range may be adversely affected by warming as physiological thresholds are exceeded (Wiens, 2016). Thermal stress can lead to mortality and consequent population-level effects, such as decreased abundance, altered size structure, local extinction and range contractions (Smale, 2020). 

Alaria esculenta is a polar to cold-temperate species that has been recorded from Brittany, France to Northern Norway (Birkett et al., 1998b). Sea temperature regulates metabolism and reproduction and defines the regional distribution of Alaria esculenta (Fredersdorf et al., 2009). The southern limit of Alaria esculenta has been defined at the 20°C isotherm (Munda & Lüning, 1977; Fredersdorf et al., 2009), however, it is more common north of the 16°C isotherm (Munda & Lüning, 1977; Van der Hoek, 1982; Kraan, 2020). As a result of this upper temperature threshold, Alaria esculenta is largely absent from the southern North Sea and the English Channel where summer temperatures exceed 16°C. 

Munda & Lüning (1977) observed temperatures of 16-17°C, sustained over 2 weeks in Helgoland, Germany, were lethal to resident Alaria esculenta. Experimental observations showed acute exposure to ≥21°C is lethal to Alaria esculenta causing bleaching and disintegration (Sundene, 1962; Fredersdorf et al., 2009). At its northern range edge (Svalbard), it is a prominent macroalga on the sublittoral fringe bedrock.  At these northern latitudes, average summer temperature can reach 5°C, with an average annual sea temperature of 3°C (1980-2014, Beszczynska-Möller & Dye, 2013). Experimental observations conducted by Fredersdorf et al. (2009) found the optimal temperature for sporophyte photosynthesis was within the range of 13-17°C, however, the optimal temperature for Alaria esculenta germination was 2-12°C (Fredersdorf et al., 2009).

A study by Zacher et al. (2019) observed gametogenesis and sporophyte formation of Alaria esculenta to be inhibited at 15°C. Zacher et al. (2019) also observed sporophyte growth to be slower at 10°C than at 4°C. Equally, Park et al. (2017) noted Alaria esculenta female gametophytes to produce more sporophytes at 5°C than at 10°C, and with no sporophytes at 15°C. However, Kraan. (2020) reports Alaria esculenta gametophytes to able to survive -1.5 to 20 °C. The literature suggests that the distribution of Alaria esculenta is possibly determined by the temperature requirements for gametogenesis or reproduction rather than the temperature tolerance of the gametophyte or sporophyte (Zacher et al., 2019; Kraan, 2020). 

Mytilus edulis is a eurytopic species found in a wide temperature range from mild, subtropical regions to areas that frequently experience freezing conditions and are vulnerable to ice scour (Seed & Suchanek 1992). In the north Atlantic, this species occurs from Norway to the coast of Spain. In the western Atlantic, Mytilus edulis is reported to be expanding its range pole-wards and has reappeared in Svalbard, due to an increase in sea temperature in that region (Berge et al., 2005). However, its equatorial limits have contracted approximately 350 km north of its previous southern limits in Cape Hatteras, North Carolina, due to increases in water temperature beyond the lethal limit (Jones et al., 2009).

In British waters 29°C was recorded as the upper sustained thermal tolerance limit for Mytilus edulis (Read & Cumming, 1967; Almada-Villela, et al., 1982), although it is thought that European mussels will rarely experience temperatures above 25°C (Seed & Suchanek, 1992). At the upper range of a mussels tolerance limit, heat shock proteins are produced, indicating high stress levels (Jones et al., 2010).  After a single day at 30°C, heat shock proteins were still present over 14 days later, although at a reduced level.  Increased temperatures can also affect reproduction in Mytilus edulis (Myrand et al., 2000).  In shallow lagoons, mortality began in late July at the end of a major spawning event when temperatures peaked at >20°C.  These mussels had a low energetic content post-spawning and had stopped shell growth.  It is likely that the high temperatures caused mortality due to the reduced condition of the mussels post-spawning (Myrand et al., 2000). Similarly, Hiebenthal et al. (2013) found that the growth rate decreased by 60% as temperatures increased from 20 - 25°C and resulted in 25% mortality under experimental conditions. Incze et al. (1980) found that Mytilus edulis growth decreased at 20°C and mortality occurred at 25°C, although mortality occurred at lower temperatures when phytoplankton abundance was low, suggesting that mortality occurred through a combination of reducing food source at a time of metabolic stress.

Rising air temperatures can also lead to significant mortality in Mytilus edulis. Intertidal ecosystems are likely to be more negatively impacted than subtidal ecosystems, due to their increased daily and seasonal variations in temperatures (Jones et al., 2009). Temperature changes may also lead to indirect effects. For example, an increase in temperature increases the mussels’ susceptibility to pathogens (Vibrio tubiashii) in the presence of relatively low concentrations of copper (Parry & Pipe, 2004).  Increased temperatures may also allow for range expansion of parasites or pathogens which will have a negative impact upon the health of the mussels if they become infected. There is evidence that increases in temperature will also give a competitive advantage to invasive species.  For example, in the Dutch Wadden Sea mild winters favour Magallana gigas recruitment while cold winters favour Mytilus edulis (Deiderich, 2005).

Alaria esculenta has already shown signs of contracting its range in the UK as a result of ocean warming (Mieszkowska, 2016). The abundance of Alaria esculenta has declined in shallow subtidal zones around the western English Channel and is predicted to disappear from south-west England and the coasts of western and southern Ireland (Mieszkowska et al., 2005; Birchenough, et al., 2013).

Corallina officinalis may tolerate between -4 to 28°C (Lüning, 1990), although when Colthart & Johansen (1973) exposed this species to a number of different temperatures, they found that growth was maintained at 18°C and ceased at 25°C. Abrupt temperature changes (10°C in California, Seapy & Littler 1984; 4.8 to 8.5°C, Hawkins & Hartnoll, 1985) resulted in dramatic declines. However, in both cases recovery was rapid, suggesting that the crustose bases survived. 

Sensitivity assessment. Alaria esculenta is nearing its southern limits in the UK, with this species only occurring as far south as Brittany, France. Sea surface temperatures (SST) around the UK currently fall between 6-19°C (Huthnance, 2010). The available evidence suggests that the effects of ocean warming may occur throughout the year.  If winter temperatures exceed 12°C this is likely to inhibit germination, whilst summer temperatures greater than 20°C will cause mortality of Alaria esculentaAlaria esculenta is competitively inferior to Laminaria digitata in the northeast Atlantic (Hawkins & Harkin, 1985) where it is confined to more exposed shores and can colonize sheltered environments only if Laminaria digitata is removed. As temperatures rise to up to 20°C, it is expected that the competitive ability of this species will decrease further, while as temperatures rise above 20°C Alaria esculenta will be lost, with more warm adapted algae taking its place. Brodie et al. (2014) predict that Alaria esculenta will be completely lost from Boreal habitats by the end of this century, whilst all kelp species will be lost from the Lusitanian region, replaced by smaller, fleshy algae.

Sea surface temperatures around the UK are currently between 6-19°C (Huthnance, 2010). Under the middle emission scenario Alaria esculenta is likely to be lost from most of the UK, although it may manage to maintain some populations in Scotland, where current summer temperatures often reach 14°C, leading to potential summer temperatures of 17°C. Corallina officinalis, Mytilus edulis and other warm-tolerant species should be able to cope with temperature increases under a middle emission scenario in UK waters. As Alaria esculenta is the main characterizing species for this study and is expected to be lost from a large portion of the UK, under this scenario resistance is assessed as ‘Low’. Resilience is assessed as ‘Very Low’, as loss is likely to be a long-term decline, due to the long-term nature of ocean warming. Therefore, this biotope IR.HIR.KFaR.Ala.Myt is assessed as having ‘High’ sensitivity to ocean warming under a middle emission scenario.

For the high emission scenario and extreme scenario, sea temperatures may rise by 4-5°C to give potential southern summer temperatures of 23-24°C and northern summer temperatures of 18-19°C. Under these scenarios, it is likely that Alaria esculenta will be lost almost completely from the UK. Therefore, resistance is assessed as ‘None’, and resilience is assessed as ‘Very low’. Overall, this biotope Ala.Myt is assessed as having ‘High’ sensitivity to ocean warming for the high emission scenario and the extreme scenario.  

Low
High
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Very Low
High
High
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High
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High
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Marine heatwaves (high) [Show more]

Marine heatwaves (high)

High emission scenario benchmark: A marine heatwave occurring every two years, with a mean duration of 120 days, and a maximum intensity of 3.5°C. Further detail.

Evidence

Marine heatwaves are extreme weather events defined as periods of extreme sea surface temperature that persists for days to months (Frölicher et al., 2018). Marine heatwaves are predicted to increase in intensity, occur more frequently and last for longer periods of time by the end of this century under both middle and high emission scenarios (Hobday et al., 2016; Frölicher et al., 2018). Marine heatwaves are known to cause significant impacts to kelp forests, particularly if a population is found towards the edge of its southern limit (Smale et al., 2019). 

In Baja California, Mexico, an extreme heat even between 2014 – 2016, led to both a decrease in density of Macrocystis pyriferaand a decrease in the number of fronds per individual in Baja California, Mexico (Arafeh-Dalmau et al., 2019). Additionally, there was a significant change to the understory algal composition, and half of the fish and invertebrates associated with this habitat disappeared. The same heatwave, coupled with a loss of starfish through disease and an increase in urchin grazing, led to the loss of > 90% of Macrocystis pyrifera from 350 km of coastline in northern California (Rogers-Bennett & Catton, 2019).

As this biotope IR.HIR.KFaR.Ala.Myt occurs on the intertidal-subtidal margin, it will experience both elevated air temperatures and seawater temperatures during a heatwave, which may lead to doubly stressful conditions (Thomsen et al., 2019). Air temperatures tend to be more variable and extreme than seawater temperatures (Helmuth et al., 2002). While the south of the UK has a mean summer daily high temperature of 21°C, temperatures can often reach ≥30°C (Met_Office, 2016). Temperature loggers on the west coast of Scotland recorded intertidal temperatures on the high shore exceeding 40°C in 7 of the 11 years it was monitored (Burrows, 2017), showing the extreme temperatures that intertidal species cope with. Following the marine heatwave of 2017/2018 in New Zealand, the intertidal bull kelp, Durvillaea poha, was lost from part of the coastline (Thomsen et al., 2019). Air temperatures are likely to lead to enhanced desiccation (Thomsen et al., 2019), although this may be partially ameliorated by wave action in this biotope Ala.Myt, as it only occurs on very exposed to moderately exposed shorelines. 

Intertidal populations of Mytilus edulis may be particularly sensitive to marine heatwaves. When submerged, a mussel’s body temperature closely approximates that of the surrounding water, whereas when emerged, body temperatures can become much higher than the surrounding air or substratum (Zippay & Helmuth, 2012). In the southern portion of its range in the USA, intertidal populations of Mytilus edulis have experienced catastrophic mortality directly associated with summer high temperatures of up to 32°C, with populations shifting their range 350 km northwards of their previous extent (Jones et al., 2009).

Air temperatures tend to be more variable and extreme than seawater temperatures (Helmuth et al., 2002). While the south of the UK has a mean summer daily high temperature of 21°C, temperatures can often reach ≥30°C (Met Office, 2016). Temperature loggers on the west coast of Scotland recorded intertidal temperatures on the high shore exceeding 40°C in seven of the 11 years it was monitored (Burrows, 2017), which shows the extreme temperatures that intertidal species have to cope with, at present. Furthermore, when exposed to high daytime temperatures, internal body temperature can far exceed air temperatures. For example, when Mytilus edulis was exposed to air temperatures of up to 34°C on the shore, body temperatures of the mussels increased to 46°C, leading to mortality (Tsuchiya, 1983).

The thermal tolerance of Mytilus edulis decreases under repeated heat stress. Therefore, this species is likely to be especially sensitive to both marine and aerial heatwaves (Seuront et al., 2019). In Japan, in 1981, mass mortality of Mytilus edulis occurred along a rocky shore as a result of unusually high temperatures, while another species of mussel (Mytilisepta virgatus, which occurred in the zone above Mytilus edulis exhibited much greater levels of heat tolerance and low mortality (Tsuchiya, 1983). Mytilus edulis is thought to be particularly susceptible to high temperatures and heatwaves in the summer, due to the low energy reserves of the organism after spawning (Tremblay et al., 1998, Myrand et al., 2000).  

Sensitivity assessment. Under the middle emission scenario, if heatwaves occurred every three years, with a maximum intensity of 2°C for 80 days by the end of this century, this could lead to summer sea temperatures reaching up to 24°C in southern England and 19°C in Scotland. Under the middle emission scenario, Alaria esculenta is likely to be lost from the southern parts of the UK (see Global warming pressure).  Any remaining populations of Alaria esculenta are likely to suffer severe mortality as a result of a heatwave of this magnitude. Similarly, some of the Mytilus edulis population may be lost in the southern UK, especially in the sublittoral fringe. Therefore, resistance has been assessed as ‘None’. As a further heatwave is likely to affect this habitat before full recovery, resilience has been assessed as ‘Low.’ Therefore, this biotope IR.HIR.KFaR.Ala.Myt is assessed as having ‘High’ sensitivity to marine heatwaves under the middle emission scenario.

Under the high emission scenario, if heatwaves occur every two years by the end of this century, reaching a maximum intensity of 3.5°C for 120 days, this could lead to the heatwave lasting the entire summer with temperatures reaching up to 26.5°C in southern England and 21.5°C in Scotland. Under the high emission scenario, Alaria esculenta is likely to be almost wiped out in the UK. Similarly, some of the Mytilus edulis population may be lost in the southern UK, especially in the sublittoral fringe. Therefore, resistance has been assessed as ‘None’. As widespread mortality may lead to a lack of viable sporophytes for recruitment, resilience has been assessed as ‘Very low.’ Therefore, this biotope Ala.Myt is assessed as having ‘High’ sensitivity to marine heatwaves under the high emission scenario.

None
Medium
Medium
High
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Very Low
High
High
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High
Medium
Medium
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Marine heatwaves (middle) [Show more]

Marine heatwaves (middle)

Middle emission scenario benchmark:  A marine heatwave occurring every three years, with a mean duration of 80 days, with a maximum intensity of 2°C. Further detail.

Evidence

Marine heatwaves are extreme weather events defined as periods of extreme sea surface temperature that persists for days to months (Frölicher et al., 2018). Marine heatwaves are predicted to increase in intensity, occur more frequently and last for longer periods of time by the end of this century under both middle and high emission scenarios (Hobday et al., 2016; Frölicher et al., 2018). Marine heatwaves are known to cause significant impacts to kelp forests, particularly if a population is found towards the edge of its southern limit (Smale et al., 2019). 

In Baja California, Mexico, an extreme heat even between 2014 – 2016, led to both a decrease in density of Macrocystis pyriferaand a decrease in the number of fronds per individual in Baja California, Mexico (Arafeh-Dalmau et al., 2019). Additionally, there was a significant change to the understory algal composition, and half of the fish and invertebrates associated with this habitat disappeared. The same heatwave, coupled with a loss of starfish through disease and an increase in urchin grazing, led to the loss of > 90% of Macrocystis pyrifera from 350 km of coastline in northern California (Rogers-Bennett & Catton, 2019).

As this biotope IR.HIR.KFaR.Ala.Myt occurs on the intertidal-subtidal margin, it will experience both elevated air temperatures and seawater temperatures during a heatwave, which may lead to doubly stressful conditions (Thomsen et al., 2019). Air temperatures tend to be more variable and extreme than seawater temperatures (Helmuth et al., 2002). While the south of the UK has a mean summer daily high temperature of 21°C, temperatures can often reach ≥30°C (Met_Office, 2016). Temperature loggers on the west coast of Scotland recorded intertidal temperatures on the high shore exceeding 40°C in 7 of the 11 years it was monitored (Burrows, 2017), showing the extreme temperatures that intertidal species cope with. Following the marine heatwave of 2017/2018 in New Zealand, the intertidal bull kelp, Durvillaea poha, was lost from part of the coastline (Thomsen et al., 2019). Air temperatures are likely to lead to enhanced desiccation (Thomsen et al., 2019), although this may be partially ameliorated by wave action in this biotope Ala.Myt, as it only occurs on very exposed to moderately exposed shorelines. 

Intertidal populations of Mytilus edulis may be particularly sensitive to marine heatwaves. When submerged, a mussel’s body temperature closely approximates that of the surrounding water, whereas when emerged, body temperatures can become much higher than the surrounding air or substratum (Zippay & Helmuth, 2012). In the southern portion of its range in the USA, intertidal populations of Mytilus edulis have experienced catastrophic mortality directly associated with summer high temperatures of up to 32°C, with populations shifting their range 350 km northwards of their previous extent (Jones et al., 2009).

Air temperatures tend to be more variable and extreme than seawater temperatures (Helmuth et al., 2002). While the south of the UK has a mean summer daily high temperature of 21°C, temperatures can often reach ≥30°C (Met Office, 2016). Temperature loggers on the west coast of Scotland recorded intertidal temperatures on the high shore exceeding 40°C in seven of the 11 years it was monitored (Burrows, 2017), which shows the extreme temperatures that intertidal species have to cope with, at present. Furthermore, when exposed to high daytime temperatures, internal body temperature can far exceed air temperatures. For example, when Mytilus edulis was exposed to air temperatures of up to 34°C on the shore, body temperatures of the mussels increased to 46°C, leading to mortality (Tsuchiya, 1983).

The thermal tolerance of Mytilus edulis decreases under repeated heat stress. Therefore, this species is likely to be especially sensitive to both marine and aerial heatwaves (Seuront et al., 2019). In Japan, in 1981, mass mortality of Mytilus edulis occurred along a rocky shore as a result of unusually high temperatures, while another species of mussel (Mytilisepta virgatus, which occurred in the zone above Mytilus edulis exhibited much greater levels of heat tolerance and low mortality (Tsuchiya, 1983). Mytilus edulis is thought to be particularly susceptible to high temperatures and heatwaves in the summer, due to the low energy reserves of the organism after spawning (Tremblay et al., 1998, Myrand et al., 2000).  

Sensitivity assessment. Under the middle emission scenario, if heatwaves occurred every three years, with a maximum intensity of 2°C for 80 days by the end of this century, this could lead to summer sea temperatures reaching up to 24°C in southern England and 19°C in Scotland. Under the middle emission scenario, Alaria esculenta is likely to be lost from the southern parts of the UK (see Global warming pressure).  Any remaining populations of Alaria esculenta are likely to suffer severe mortality as a result of a heatwave of this magnitude. Similarly, some of the Mytilus edulis population may be lost in the southern UK, especially in the sublittoral fringe. Therefore, resistance has been assessed as ‘None’. As a further heatwave is likely to affect this habitat before full recovery, resilience has been assessed as ‘Low.’ Therefore, this biotope IR.HIR.KFaR.Ala.Myt is assessed as having ‘High’ sensitivity to marine heatwaves under the middle emission scenario.

Under the high emission scenario, if heatwaves occur every two years by the end of this century, reaching a maximum intensity of 3.5°C for 120 days, this could lead to the heatwave lasting the entire summer with temperatures reaching up to 26.5°C in southern England and 21.5°C in Scotland. Under the high emission scenario, Alaria esculenta is likely to be almost wiped out in the UK. Similarly, some of the Mytilus edulis population may be lost in the southern UK, especially in the sublittoral fringe. Therefore, resistance has been assessed as ‘None’. As widespread mortality may lead to a lack of viable sporophytes for recruitment, resilience has been assessed as ‘Very low.’ Therefore, this biotope Ala.Myt is assessed as having ‘High’ sensitivity to marine heatwaves under the high emission scenario.

None
Medium
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Low
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High
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Medium
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Ocean acidification (high) [Show more]

Ocean acidification (high)

High emission scenario benchmark: a further decrease in pH of 0.35 (annual mean) and corresponding 120% increase in H+ ions , seasonal aragonite saturation of 20% of UK coastal waters and North Sea bottom waters, and the aragonite saturation horizon in the NE Atlantic, off the continental shelf, occurring at a depth of 400 m by the end of this century 2081-2100. Further detail 

Evidence

Increasing levels of CO2 in the atmosphere have led to the average pH of sea surface waters dropping from 8.25 in the 1700s to 8.14 in the 1990s (Jacobson, 2005), with it expected to drop up to a further 0.35 units by the end of this century, dependent on the emission scenario. Marine autotrophs will generally benefit from ocean acidification, through an increase in the availability of aqueous COfor photosynthesis (Koch et al., 2013). Most species of kelp appear to be under-saturated in respect to carbon dioxide, although they can generally utilise HCO3 and have external carbonic anhydrase for extracellular dehydration of HCO3 to CO2 (Koch et al., 2013). 

Under experimental conditions, Iñiguez et al. (2016a) found that although photosynthesis remained stable in Alaria esculenta in response to increasing CO2, and the growth rate increased. Similarly, Gordillo et al. (2015) found heightened growth rates in Alaria esculenta when exposed to increased CO2, although this increase was not significant and less pronounced than in Saccharina lattisima.  Research on other kelp species has revealed a positive or neutral effect of ocean acidification (Roleda et al., 2012, Fernández et al., 2015, Nunes et al., 2015, Iñiguez et al., 2016a, b), except for one study, which found that ocean acidification negatively impacted photosynthesis and growth in the southern hemisphere species, Ecklonia radiata (Britton et al., 2016). 

In general, it is thought that calcifying invertebrates will be more sensitive to ocean acidification than non-calcifying invertebrates, which appear to have a more mixed response (Hofmann et al., 2010), although bivalves generally appear to be tolerant to a decrease in pH (Kroeker et al., 2011, Garrard et al., 2014). Mytilus edulis is a calcified organism but it is unlikely this species will be significantly negatively impacted by ocean acidification, because acidification does not appear to lead to mortality, even at levels which far exceed levels of ocean acidification expected for the end of this century (e.g. Berge et al., 2006, Melzner et al., 2011). For example, levels of growth in Mytilus edulis were maintained at pH 7.6 -7.7, and growth did decrease under pH levels < 7.4 (Berge et al., 2006, Melzner et al., 2011).

The calcified shell of Mytilus edulis consists of an outer calcite layer and an inner aragonite layer (Fitzer et al., 2015). When cultured at levels of acidification expected for the end of this century under both the middle (550 ppm) and high (1000 ppm) emission scenario, results showed that Mytilus edulis shells became more brittle (Fitzer et al., 2015). There was no impact of ocean acidification on the production or strength of the byssal threads (Dickey et al., 2018). Beesley et al. (2008) found that the health of Mytilus edulis decreased as a result of 60 days exposure to increased CO2, which they suggested was due to the elevated concentration of calcium ions in the haemolymph. Sun et al. (2017) found that ocean acidification damaged the ultrastructure of haemocytes and led to a reduction in phagocytosis.

Corallina officinalis is a highly calcified, erect, red algae. Results of experimental COenrichment suggest that this species could be significantly negatively affected by future ocean acidification. Hofmann et al. (2012) found that growth and photosynthesis decreased as a result of a 0.3 unit decrease in pH. Further investigation showed that skeletal CaCO3 decreased with increasing COat levels expected for both the middle emission and high emission scenarios, although this decrease was small (< 2%) (Hofmann et al., 2013). Yildiz et al. (2013) showed that although CaCO3 decreased in Corallina officinalis as a result of ocean acidification, photosynthesis increased. When ocean acidification was combined with an increase in UV radiation, which led to an increase in growth rate. They summarised that a decrease in CaCO3 content may not be negative but may lead to this species absorbing and using light differently. Brodie et al. (2014) report Corallina species to be more resilient to ocean acidification than other calcified algae species, although competition from flesh algal species that benefit from high CO2 may indirectly cause the loss of calcified species from biotopes. Similarly, observations have indicated Corallinales to be adversely affected at locations where CO2 gradients occur naturally, with evidence of Corallinales being outcompeted by heterokont algae at Mediterranean CO2 seeps (Martin & Hall-Spencer, 2017).  

Sensitivity assessment. Kelp forests occur in a naturally variable pH habitat, with diel fluctuations of 0.3 - 0.45 pH units (Krause-Jensen et al., 2015, Britton et al., 2016), and boundary layer pH fluctuation of up to 0.8 units (Krause-Jensen et al., 2015). Alaria esculenta is not expected to suffer negative impacts from future acidification, and whilst calcium carbonate content of Corallina officinalis may reduce as a result of acidification, this species is expected to survive future COenrichment of the oceans. In addition, Mytilus edulis is unlikely to be significantly negatively impacted by ocean acidification. Therefore, under both the middle and high emission scenario resistance is assessed as ‘High', and resilience as ‘High’, leading to a sensitivity of ‘Not sensitive’.

Medium
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Medium
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High
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Low
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Ocean acidification (middle) [Show more]

Ocean acidification (middle)

Middle emission scenario benchmark: a further decrease in pH of 0.15 (annual mean) and corresponding 35% increase in H+ ions with no coastal aragonite undersaturation and the aragonite saturation horizon in the NE Atlantic, off the continental shelf, at a depth of 800 m by the end of this century 2081-2100. Further detail.

Evidence

Increasing levels of CO2 in the atmosphere have led to the average pH of sea surface waters dropping from 8.25 in the 1700s to 8.14 in the 1990s (Jacobson, 2005), with it expected to drop up to a further 0.35 units by the end of this century, dependent on the emission scenario. Marine autotrophs will generally benefit from ocean acidification, through an increase in the availability of aqueous COfor photosynthesis (Koch et al., 2013). Most species of kelp appear to be under-saturated in respect to carbon dioxide, although they can generally utilise HCO3 and have external carbonic anhydrase for extracellular dehydration of HCO3 to CO2 (Koch et al., 2013). 

Under experimental conditions, Iñiguez et al. (2016a) found that although photosynthesis remained stable in Alaria esculenta in response to increasing CO2, and the growth rate increased. Similarly, Gordillo et al. (2015) found heightened growth rates in Alaria esculenta when exposed to increased CO2, although this increase was not significant and less pronounced than in Saccharina lattisima.  Research on other kelp species has revealed a positive or neutral effect of ocean acidification (Roleda et al., 2012, Fernández et al., 2015, Nunes et al., 2015, Iñiguez et al., 2016a, b), except for one study, which found that ocean acidification negatively impacted photosynthesis and growth in the southern hemisphere species, Ecklonia radiata (Britton et al., 2016). 

In general, it is thought that calcifying invertebrates will be more sensitive to ocean acidification than non-calcifying invertebrates, which appear to have a more mixed response (Hofmann et al., 2010), although bivalves generally appear to be tolerant to a decrease in pH (Kroeker et al., 2011, Garrard et al., 2014). Mytilus edulis is a calcified organism but it is unlikely this species will be significantly negatively impacted by ocean acidification, because acidification does not appear to lead to mortality, even at levels which far exceed levels of ocean acidification expected for the end of this century (e.g. Berge et al., 2006, Melzner et al., 2011). For example, levels of growth in Mytilus edulis were maintained at pH 7.6 -7.7, and growth did decrease under pH levels < 7.4 (Berge et al., 2006, Melzner et al., 2011).

The calcified shell of Mytilus edulis consists of an outer calcite layer and an inner aragonite layer (Fitzer et al., 2015). When cultured at levels of acidification expected for the end of this century under both the middle (550 ppm) and high (1000 ppm) emission scenario, results showed that Mytilus edulis shells became more brittle (Fitzer et al., 2015). There was no impact of ocean acidification on the production or strength of the byssal threads (Dickey et al., 2018). Beesley et al. (2008) found that the health of Mytilus edulis decreased as a result of 60 days exposure to increased CO2, which they suggested was due to the elevated concentration of calcium ions in the haemolymph. Sun et al. (2017) found that ocean acidification damaged the ultrastructure of haemocytes and led to a reduction in phagocytosis.

Corallina officinalis is a highly calcified, erect, red algae. Results of experimental COenrichment suggest that this species could be significantly negatively affected by future ocean acidification. Hofmann et al. (2012) found that growth and photosynthesis decreased as a result of a 0.3 unit decrease in pH. Further investigation showed that skeletal CaCO3 decreased with increasing COat levels expected for both the middle emission and high emission scenarios, although this decrease was small (< 2%) (Hofmann et al., 2013). Yildiz et al. (2013) showed that although CaCO3 decreased in Corallina officinalis as a result of ocean acidification, photosynthesis increased. When ocean acidification was combined with an increase in UV radiation, which led to an increase in growth rate. They summarised that a decrease in CaCO3 content may not be negative but may lead to this species absorbing and using light differently. Brodie et al. (2014) report Corallina species to be more resilient to ocean acidification than other calcified algae species, although competition from flesh algal species that benefit from high CO2 may indirectly cause the loss of calcified species from biotopes. Similarly, observations have indicated Corallinales to be adversely affected at locations where CO2 gradients occur naturally, with evidence of Corallinales being outcompeted by heterokont algae at Mediterranean CO2 seeps (Martin & Hall-Spencer, 2017).  

Sensitivity assessment. Kelp forests occur in a naturally variable pH habitat, with diel fluctuations of 0.3 - 0.45 pH units (Krause-Jensen et al., 2015, Britton et al., 2016), and boundary layer pH fluctuation of up to 0.8 units (Krause-Jensen et al., 2015). Alaria esculenta is not expected to suffer negative impacts from future acidification, and whilst calcium carbonate content of Corallina officinalis may reduce as a result of acidification, this species is expected to survive future COenrichment of the oceans. In addition, Mytilus edulis is unlikely to be significantly negatively impacted by ocean acidification. Therefore, under both the middle and high emission scenario resistance is assessed as ‘High', and resilience as ‘High’, leading to a sensitivity of ‘Not sensitive’.

High
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Medium
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High
High
High
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Not sensitive
High
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Sea level rise (extreme) [Show more]

Sea level rise (extreme)

Extreme scenario benchmark: a 107 cm rise in average UK by the end of this century (2018-2100). Further detail.

Evidence

Sea-level rise is occurring through a combination of thermal expansion and ice melt.  Sea levels have risen 1-3 mm/yr in the last century (Cazenave & Nerem, 2004, Church et al., 2004, Church & White, 2006). Sea-level rise is expected to lead to substantial loss of intertidal habitats. Rocky shores backed by cliffs constitute about 80% of oceanic coastlines globally and in Britain, 42% of the coastline is hard rock, with many areas having cliffs behind the shore (Jackson & McIlvenny, 2011).

Jackson & McIlvenny (2011) predicted that under a 30 cm sea-level rise, between 10 - 27% of the extent of intertidal rocky shores in Scotland would be lost, whilst under a 190 cm sea-level rise, between 26 - 50% would be lost. Using a modelling-based approach, Kaplanis et al. (2019) found that in San Diego County loss of intertidal habitat would be most extreme within the first metre of sea-level rise, with 29.9% of intertidal rocky shore lost as a result of a 20 cm sea-level rise, and 77.7% as a result of a 100 cm sea-level rise.

Sensitivity assessment. This biotope IR.HIR.KFaR.Ala.Myt is found on very exposed fringe bedrock on the lower shore and shallow subtidal, and therefore an increase in sea level height of 50, 70 and 107 cm could have severe repercussions for the extent of this biotope. Beds may be able to expand their range and migrate upwards to compensate for sea-level rise, if not constrained by lack of suitable habitat (IPCC, 2019). In this assessment we have assessed on a worst-case-scenario basis, assuming that landward migration is not possible, which is likely to lead to the depth distribution of Alaria esculenta and Mytilus edulis shrinking significantly in response to a 50, 70 or 107 cm sea-level rise, without the possibility of recovery. Alaria esculenta is generally limited to a depth of 1-2 m, as below this depth it is usually outcompeted by Laminaria hyperborea. As depth increases due to sea-level rise, Laminaria hyperborea is likely to extend its distribution shorewards. 

Under the middle emission, high emission and extreme scenarios (50, 70 and 107 cm sea-level rise), it is expected that between 25 - 75% of this biotope is likely to be lost.  Therefore, for all three scenarios, resistance has been assessed as ‘Low’, and resilience as ‘Very low’, and sensitivity is assessed as ‘High’.

Low
Low
NR
NR
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Very Low
High
High
High
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High
Low
Low
Low
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Sea level rise (high) [Show more]

Sea level rise (high)

High emission scenario benchmark: a 70 cm rise in average UK by the end of this century (2018-2100). Further detail.

Evidence

Sea-level rise is occurring through a combination of thermal expansion and ice melt.  Sea levels have risen 1-3 mm/yr in the last century (Cazenave & Nerem, 2004, Church et al., 2004, Church & White, 2006). Sea-level rise is expected to lead to substantial loss of intertidal habitats. Rocky shores backed by cliffs constitute about 80% of oceanic coastlines globally and in Britain, 42% of the coastline is hard rock, with many areas having cliffs behind the shore (Jackson & McIlvenny, 2011).

Jackson & McIlvenny (2011) predicted that under a 30 cm sea-level rise, between 10 - 27% of the extent of intertidal rocky shores in Scotland would be lost, whilst under a 190 cm sea-level rise, between 26 - 50% would be lost. Using a modelling-based approach, Kaplanis et al. (2019) found that in San Diego County loss of intertidal habitat would be most extreme within the first metre of sea-level rise, with 29.9% of intertidal rocky shore lost as a result of a 20 cm sea-level rise, and 77.7% as a result of a 100 cm sea-level rise.

Sensitivity assessment. This biotope IR.HIR.KFaR.Ala.Myt is found on very exposed fringe bedrock on the lower shore and shallow subtidal, and therefore an increase in sea level height of 50, 70 and 107 cm could have severe repercussions for the extent of this biotope. Beds may be able to expand their range and migrate upwards to compensate for sea-level rise, if not constrained by lack of suitable habitat (IPCC, 2019). In this assessment we have assessed on a worst-case-scenario basis, assuming that landward migration is not possible, which is likely to lead to the depth distribution of Alaria esculenta and Mytilus edulis shrinking significantly in response to a 50, 70 or 107 cm sea-level rise, without the possibility of recovery. Alaria esculenta is generally limited to a depth of 1-2 m, as below this depth it is usually outcompeted by Laminaria hyperborea. As depth increases due to sea-level rise, Laminaria hyperborea is likely to extend its distribution shorewards. 

Under the middle emission, high emission and extreme scenarios (50, 70 and 107 cm sea-level rise), it is expected that between 25 - 75% of this biotope is likely to be lost.  Therefore, for all three scenarios, resistance has been assessed as ‘Low’, and resilience as ‘Very low’, and sensitivity is assessed as ‘High’.

Low
Low
NR
NR
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Very Low
High
High
High
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High
Low
Low
Low
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Sea level rise (middle) [Show more]

Sea level rise (middle)

Middle emission scenario benchmark: a 50 cm rise in average UK sea-level rise by the end of this century (2081-2100). Further detail.

Evidence

Sea-level rise is occurring through a combination of thermal expansion and ice melt.  Sea levels have risen 1-3 mm/yr in the last century (Cazenave & Nerem, 2004, Church et al., 2004, Church & White, 2006). Sea-level rise is expected to lead to substantial loss of intertidal habitats. Rocky shores backed by cliffs constitute about 80% of oceanic coastlines globally and in Britain, 42% of the coastline is hard rock, with many areas having cliffs behind the shore (Jackson & McIlvenny, 2011).

Jackson & McIlvenny (2011) predicted that under a 30 cm sea-level rise, between 10 - 27% of the extent of intertidal rocky shores in Scotland would be lost, whilst under a 190 cm sea-level rise, between 26 - 50% would be lost. Using a modelling-based approach, Kaplanis et al. (2019) found that in San Diego County loss of intertidal habitat would be most extreme within the first metre of sea-level rise, with 29.9% of intertidal rocky shore lost as a result of a 20 cm sea-level rise, and 77.7% as a result of a 100 cm sea-level rise.

Sensitivity assessment. This biotope IR.HIR.KFaR.Ala.Myt is found on very exposed fringe bedrock on the lower shore and shallow subtidal, and therefore an increase in sea level height of 50, 70 and 107 cm could have severe repercussions for the extent of this biotope. Beds may be able to expand their range and migrate upwards to compensate for sea-level rise, if not constrained by lack of suitable habitat (IPCC, 2019). In this assessment we have assessed on a worst-case-scenario basis, assuming that landward migration is not possible, which is likely to lead to the depth distribution of Alaria esculenta and Mytilus edulis shrinking significantly in response to a 50, 70 or 107 cm sea-level rise, without the possibility of recovery. Alaria esculenta is generally limited to a depth of 1-2 m, as below this depth it is usually outcompeted by Laminaria hyperborea. As depth increases due to sea-level rise, Laminaria hyperborea is likely to extend its distribution shorewards. 

Under the middle emission, high emission and extreme scenarios (50, 70 and 107 cm sea-level rise), it is expected that between 25 - 75% of this biotope is likely to be lost.  Therefore, for all three scenarios, resistance has been assessed as ‘Low’, and resilience as ‘Very low’, and sensitivity is assessed as ‘High’.

Low
Low
NR
NR
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Very Low
High
High
High
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High
Low
Low
Low
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Hydrological Pressures

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Temperature increase (local) [Show more]

Temperature increase (local)

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

Evidence

Alaria esculenta is a northern/boreal species that has been recorded from Brittany, France to Northern Norway (Birkett et al., 1998). Sea temperature regulates metabolism and reproduction, and defines the regional distribution of Alaria esculenta (Fredersdorf et al., 2009).  The southern limit of Alaria esculenta has been defined at the 20°C isotherm (Munda & Lüning, 1977; Fredersdorf et al., 2009), however, it is common north of the 16°C isotherm (Munda & Lüning, 1977). As a result of this upper temperature threshold, Alaria esculenta is largely absent from the southern North Sea and English channel where summer temperatures can exceed 16°C.

Munda & Lüning (1977) observed temperatures of 16-17°C sustained over 2 weeks in Helgoland, Germany, were lethal to resident Alaria esculenta. Experimental observations showed that acute exposure to ≥21°C is lethal to Alaria esculenta causing bleaching and disintegration (Sundene, 1962; Fredersdorf et al., 2009). At its northern range edge (Svalbard) it is a prominent macroalgae on sublittoral fringe bedrock.  At these latitudes, average summer temperature can reach 5°C, with an average annual sea temperature of 3°C (1980-2014, Beszczynska-Möller & Dye, 2013). Experimental observations conducted by Fredersdorf et al., (2009) found the optimal temperature for sporophyte photosynthesis was within the range of 13-17°C, however, the optimal temperature for Alaria esculenta germination is 2-12°C (Fredersdorf et al., 2009).

Alaria esculenta has an approximate mid-range within southern Norway (60 deg to 65 deg North) (Birkett et al., 1998b), and as such IR.HIR.KFaR.Ala and IR.HIR.KFaR.AlaAnCrSp (plus associated sub-biotopes) have a southerly distribution when considering the geographic distribution of Alaria esculenta. Throughout the UK northern to southern Sea Surface Temperature (SST) ranges from 8-16°C in summer and 6-13°C in winter (Beszczynska-Möller & Dye, 2013). The available evidence suggests that the effects of an increase in temperature would be seasonally variable, with higher impacts during periods of spore release (Nov-march) and germination. A 5°C increase in temperature for one month may cause high mortality, limit photosynthetic ability plus germination rates.  A 2°C increase in temperature for one year may limit germination; however sporophyte photosynthetic ability may not be dramatically affected. Temperature increases of 2 or 5°C at the southern extreme of Alaria esculenta’ range (Brittany, France) is likely to cause high mortality.

Corallina officinalis may tolerate between minus 4 to 28°C (Lüning, 1990). Abrupt temperature changes (10°C in California, Seapy & Littler 1984; 4.8 to 8.5°C, Hawkins & Hartnoll, 1985) resulted in dramatic declines. However, in both cases recovery was rapid, suggesting that the crustose bases survived. Therefore, both Alaria esculenta and Corallina officinalis are probably intolerant of acute short-term temperature change of 5°C for a month. Long-term change of 2°C may reduce the southern limit of the population of Alaria esculenta.

Sensitivity assessment. Resistance to the pressure is considered ’None‘, and resilience ’High‘. The sensitivity of this biotope to an increase in temperature has been assessed as ’Medium‘. This sensitivity assessment takes into account a temperature increase of 5°C for one month. The effects of a 2°C increase in temperature for one year is likely to have less of an impact. In the later scenario, resistance would be assessed as “Medium”, and resilience “High”. Sensitivity would be assessed as “Low”.

None
Medium
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High
High
Low
High
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Medium
Medium
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Temperature decrease (local) [Show more]

Temperature decrease (local)

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

Evidence

Alaria esculenta is a northern/boreal species that has been recorded from Brittany, France to Northern Norway (Birkett et al., 1998). Sea temperature has been cited as an influential abiotic stressor; responsible for regulating metabolism and reproduction, plus defining the regional distribution of Alaria esculenta (Fredersdorf et al., 2009). At Alaria’s northern range edge (Svalbard) it is a prominent macro-algae on sublittoral fringe bedrock. At these latitudes, average summer temperature can reach 5°C, and average annual sea temperature 3°C (1980-2014, Beszczynska-Möller & Dye, 2013). Experimental observations conducted by Fredersdorf et al., (2009) found the optimal temperature for sporophyte photosynthesis was within the range of 13-17°C, however, the optimal temperature for Alaria esculenta germination is 2-12°C°C (Fredersdorf et al., 2009).

Alaria esculenta has an approximate mid-range within southern Norway (60 deg to 65 deg North) (Birkett et al., 1998b), and as such IR.HIR.KFaR.Ala and IR.HIR.KFaR.AlaAnCrSp (plus associated sub-biotopes) have a southerly distribution when considering the geographic distribution of Alaria esculenta. Throughout the UK northern to southern Sea Surface Temperature (SST) ranges from 8-16°C in summer and 6-13°C in winter (Beszczynska-Möller & Dye, 2013). A 5°C decrease in temperature for one month at Alaria esculenta’ approximate mid-range may affect the photosynthetic ability of sporophytes, however not impact germination and hence recruitment. A 2°C increase in temperature for one year at Alaria esculenta’ approximate mid-range is not likely to significantly affect Alaria esculenta.

Sensitivity assessment. Resistance to the pressure is considered ’High‘, and resilience ’High‘. The sensitivity of this biotope to an increase in temperature has been assessed as ’Not Sensitive‘. 

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Not sensitive
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Salinity increase (local) [Show more]

Salinity increase (local)

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

Evidence

Lüning (1990) suggest that “kelps” are stenohaline, their general tolerance to salinity as a phenotypic group covering 16-50 psu over a 24 hr period. Optimal growth probably occurs between 30-35 psu (MNCR category-Full Salinity) and growth rates are likely to be affected by periodic salinity stress.

Karsten (2007) tested the photosynthetic ability of Alaria esculenta under acute 2 & 5 day exposure to salinity treatments ranging from 5-60 psu. A control experiment was also carried at 34 PSU. Between 10-50 psu Alaria esculenta showed high photosynthetic ability at 83-94% of the control. Hypersaline treatments with 55-60 psu led to a 30% reduction in photosynthetic ability, ~70% of the control level. At 5 psu Alaria esculenta showed a low photosynthetic ability at 15.8% of the control. After 5 days at 5 psu all Alaria esculenta specimens were bleached and none survived. Karsten (2007) suggested that Alaria esculenta photosynthetic ability is highly affected by acute exposure to hyposaline conditions (<10 psu). The effect of long-term salinity changes (>5 days) or the effect of salinity >60 psu on Alaria esculenta’ photosynthetic ability was not tested. The experiment was conducted in the Arctic, and the authors suggest that at extremely low water temperatures (1-5°C) macro-algal acclimation to rapid salinity changes could be slower than at temperate latitudes. It is therefore possible that Alaria esculenta maybe be able to acclimate to salinity changes more effectively and quicker in UK waters, however evidence for this is limited.

Corallina officinalis is restricted to full salinity waters in the Baltic and grows maximally between 33 and 38 psu in Texan lagoons (Kinne 1971). This biotope is likely to be exposed to short-term freshwater runoff at low tide but is likely to be intolerant of long-term changes in salinity, which are likely to depress its upper limit and reduce the extent of the population.

Sensitivity assessment. IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes have been recorded exclusively in full salinity (30-40‰) (Connor et al., 2004). Karsten (2007) suggests that at salinities ranging from 10-50 psu Alaria esculenta photosynthetic ability was high. At salinities >50 psu photosynthetic ability was reduced by 30% but no mortality of the specimens was recorded. Resistance to the pressure is considered ’Medium‘, as other characterizing species (e.g. sponges, ascidians) are likely to be more sensitive to hypersaline conditions and resilience ’High’. The sensitivity of this biotope to an increase in salinity has been assessed as ’Low’.

Medium
Medium
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High
High
Low
High
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Low
Medium
Low
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Salinity decrease (local) [Show more]

Salinity decrease (local)

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

Evidence

Lüning (1990) suggest that “kelps” are stenohaline, their general tolerance to salinity as a phenotypic group covering 16-50 psu over a 24 hr period. Optimal growth probably occurs between 30-35 psu (MNCR category Full Salinity) and growth rates are likely to be affected by periodic salinity stress.

Karsten (2007) tested the photosynthetic ability of Alaria esculenta under acute 2 & 5 day exposure to salinity treatments ranging from 5-60 psu. A control experiment was also carried at 34 PSU. Between 10-50 psu Alaria esculenta showed high photosynthetic ability at 83-94% of the control. Hypersaline treatments with 55-60 psu led to a 30% reduction in photosynthetic ability, ~70% of the control level. At 5 psu Alaria esculenta showed a low photosynthetic ability at 15.8% of the control. After 5 days at 5 psu all Alaria esculenta specimens were bleached and none survived. Karsten (2007) suggested that Alaria esculenta photosynthetic ability is highly affected by acute exposure to hyposaline conditions (<10 psu). The effect of long-term salinity changes (>5 days) or the effect of salinity >60 psu on Alaria esculenta’ photosynthetic ability was not tested. The experiment was conducted in the Arctic, and the authors suggest that at extremely low water temperatures (1-5°C) macro-algal acclimation to rapid salinity changes could be slower than at temperate latitudes. It is, therefore, possible that Alaria esculenta maybe be able to acclimate to salinity changes more effectively and quicker in UK waters, however evidence for this is limited.

Corallina officinalis is restricted to full salinity waters in the Baltic and grows maximally between 33 and 38 psu in Texan lagoons (Kinne 1971). This biotope is likely to be exposed to short-term freshwater runoff at low tide but is likely to be intolerant of long-term changes in salinity, which are likely to depress its upper limit and reduce the extent of the population.

Sensitivity assessment. IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes have been recorded exclusively in full salinity (30-40‰) (Connor et al., 2004). Karsten (2007) suggests that at salinities ranging from 10-50 PSU Alaria esculenta photosynthetic ability was high. At 5 PSU Alaria esculenta showed a dramatic decline in photosynthetic ability and after 5 days specimens bleached and did not survive. Sundene (1962) also noted that Alaria esculenta sporophytes grew poorly below 25 PSU. A decrease of 1 MNCR salinity scale to “Reduced Salinity” (18-30‰) may reduce growth rates, however not cause high mortality of Alaria esculenta. Resistance to the pressure is therefore considered ’Medium‘, as other characterizing species (e.g. sponges, ascidians) are likely to be more sensitive to hyposaline conditions, and resilience ’High‘.  The sensitivity of this biotope to an increase in salinity has been assessed as ’Low’.

Medium
Medium
High
High
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High
High
Low
High
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Low
Medium
Low
High
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Water flow (tidal current) changes (local) [Show more]

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

Alaria esculenta dominates the sublittoral fringe in areas exposed to severe wave action or where water surges along the sides of gullies/steep bedrock faces (Lewis, 1964; Connor et al., 2004). The high wave exposure that defines IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes damages other laminarians, and generally excludes them.  In less wave exposed locations Alaria esculenta is out-competed by other laminarians, e.g. Laminaria digitata and Laminaria hyperborea (Connor et al., 2004).IR.HIR.KFaR.AlaAnCrSp and IR.HIR.KFaR.Ala plus associated sub-biotopes are recorded within moderately strong (0.5-1.5 m/sec)-weak (<0.5m/sec) tidal streams, but have been recorded in very strong (>3 m/sec) tidal streams. Therefore, while elevated tidal flows (>3 m/sec) may increase Alaria esculenta dislodgment (Birket et al., 1998).

Increased tidal flow may remove fronds of Corallina officinalis however calcification is thought to be an adaptation to mechanical damage (Littler & Kauker 1984). Increases in water flow rate may facilitate the colonization of filter feeding organisms within the understorey and IR.HIR.KFaR.Ala.Myt may dominate over IR.HIR.KFaR.Ala.Ldig. Decreases in water flow are likely to have the opposite effect (Connor et al. 2004). Changes in the water flow regimes under kelp canopies can modify larval supply and settlement (Eckman, 1983), and affect the growth and survival of Mytillus edulis (Eckman & Duggins, 1991). Mytillus edulis settlement has been found significantly higher in close proximity to Alaria esculenta and is thought to increase beneath the canopy (Bégin et al., 2004). Therefore any loss of Alaria esculenta, as a result of changes to local water movements, may affect Mytilus edulis recruitment.

Sensitivity assessment. IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes are found in a wide range of tidal flows but exclusively in wave disturbed areas, which generally exclude other laminarians. Changes in tidal flow are not likely to independently affect the dominance of Alaria esculenta, however, may affect the understorey community.  Nevertheless, wave exposure is the dominant source of water movement in theses biotope, and a change in water flow of 0.1-0.2 m/s is unlikely to be significant. Therefore, resistance has been assessed as ’High‘ and resilience ’High‘. Sensitivity has been assessed as ’Not Sensitive‘ at the benchmark level.

Medium
Low
NR
NR
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High
High
Low
High
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Low
Low
NR
NR
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Emergence regime changes [Show more]

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

An increase in emergence will result in an increased risk of desiccation. Increased immersion may allow IR.HIR.KFaR.Ala biotopes to extend higher up the shore. However, Alaria esculenta forest will come under increased competition from Laminaria hyperborea in the shallow infralittoral. In this scenario IR.HIR.KFaR.Ala biotope distribution may shift on the shore, however, biotope structure will remain.

Alaria esculenta may extend into the lower eulittoral in extremely wave exposed conditions. However, these marginal populations have a reduced age range in comparison to subtidal populations due to desiccation increasing mortality of Alaria esculenta at low tide. An increase in desiccation is likely to remove Alaria esculenta. The resultant loss of canopy would expose Corallina officinalis turf and macrofaunal crust to desiccation and/or damage by high light intensity (bleaching). Hawkins & Harkin (1985) noted that encrusting corallines and Corallina officinalis often die when their protective algal canopy is removed. Severe damage was noted in Corallina officinalis as a result of unusually hot and sunny weather in the UK summer 1983 (Hawkins & Hartnoll, 1985). Laminaria digitata is likely to be intolerant of desiccation and destruction of its meristem (base of the blade), caused by increased wave action at low tide, will kill the sporophyte. Therefore, both IR.HIR.KFaR.Ala.Myt and IR.HIR.KFaR.Ala.Ldig are likely to be highly intolerant of increases in desiccation and the upper limit of the population would be depressed. Desiccation is unlikely to be relevant in IR.HIR.KFaR.AlaAnCrSp due to its depth (15-35m BCD) (Connor et al., 2004).

Sensitivity assessment. Resistance to this pressure is considered ’Low‘, and resilience ’High‘. The sensitivity of this biotope to a change in emergence is considered as ’Low‘.  

Low
Low
NR
NR
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High
High
Low
High
Help
Low
Low
NR
NR
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Wave exposure changes (local) [Show more]

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

Alaria esculenta dominates the sublittoral fringe in areas exposed to severe wave action or where water surges along the sides of gullies (Lewis, 1964). A decrease in local wave height will increase spatial competition from other laminarians (Connor et al., 2004). Increased wave exposure may remove fronds of Corallina officinalis however calcification is thought to an adaptation to mechanical damage (Little & Kauker 1984) and the fronds grow as a compact (short) turf in wave exposed conditions.

IR.HIR.KFaR.AlaAnCrSp occurs at one site, Rockall, Scotland where extreme oceanic swell excludes Laminaria hyperborea in the infralittoral from 14-35 m. IR.HIR.KFaR.Ala.Myt occurs predominantly on sub-littoral fringe bedrock in very exposed to exposed wave exposure.  Extremely wave exposed variants of IR.HIR.KFaR.Ala.Myt can extend to 15 m BCD where Alaria esculenta replaces Laminaria hyperborea as the assemblage dominant, and Mytillus edulis is a common understorey species in the sublittoral fringe variant (Bégin et al., 2004, Connor et al., 2004) but as depth increases Tubularia spp. becomes more abundant. IR.HIR.KFaR.Ala.Ldig occurs predominately at exposed-moderately wave exposed sites, where Laminaria digitata can spatially compete with Alaria esculenta (Connor et al., 2004).

Sensitivity assessment. The abundance of Alaria esculenta is highly affected by the degree of wave exposure at a site. Within IR.HIR.KFaR.Ala, increasing wave exposure may favour IR.HIR.KFaR.Ala.Myt over IR.HIR.KFaR.Ala.Ldig (Connor et al. 2004). Further increases in wave exposure may cause damage to Laminaria hyperborea, allowing Alaria esculenta to dominate the infralittoral. Kelp clearance experiments have shown that at moderate or lower wave exposure sites Laminaria digitata can out-compete Alaria esculenta so that a decrease in wave exposure is likely to result in loss of the Alaria dominated biotopes. Alaria dominated biotopes are therefore, sensitive to any activity or event that reduces incident wave energy.  However, a change of 3-5% in significant wave height (the benchmark) is unlikely to be significant in the wave exposed conditions favoured by theses biotopes.  Therefore, resistance is recorded as ‘High’, with a ‘High’ resilience, resulting is an assessment of ‘Not sensitive’ at the benchmark level.

None
High
High
High
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High
High
Low
High
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Medium
High
Low
High
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Chemical Pressures

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ResistanceResilienceSensitivity
Transition elements & organo-metal contamination [Show more]

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.

Johnston & Roberts (2009) conducted a meta-analysis, which reviewed 216 papers to assess how a variety of contaminants (including metal contamination) affected six marine habitats (including intertidal and subtidal reefs). A 30-50% reduction in species diversity and richness was identified from all habitats exposed to the contaminant types. Johnston & Roberts (2009) also highlighted that macroalgal communities are relatively tolerant to contamination but that metal and nutrient impacted intertidal communities can have low diversity assemblages which are dominated by opportunistic and fast growing species (Johnston & Roberts, 2009 and references therein).

Mercury (organic > inorganic) is highly toxic to macrophytes (Bryan 1984; Cole et al. 1999). Mercury and copper were lethal at 0.05 mg/l and 0.1 mg/l respectively and toxic at 0.05 mg/l and 0.01 mg/l respectively in Laminaria hyperborea. Zinc and Cadmium were lethal at 5 mg/l and 10 mg/l respectively. The presence of alginates in kelp tissue is thought to sequester heavy metals in a biologically unavailable form. It is likely that laminarians such as Alaria esculenta are relatively tolerant of heavy metals except at high concentrations at high levels. Little information on heavy metal tolerance of corallines was found.

Not Assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Hydrocarbon & PAH contamination [Show more]

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.

The mucilaginous coating on kelp fronds is thought to protect them from coatings of oil. Hydrocarbons in solution reduce photosynthesis and may be algicidal. Reduction in photosynthesis is dependent on the type of oil, its concentration and length of exposure, oil-water mixture and irradiance in experimental trials (Lobban & Harrison, 1994). Subtidal populations are only exposed to oil emulsions or oil adsorbed particles. Kelps are relatively insensitive to dispersants (Birkett et al. 1998) e.g. Laminaria digitata exposed to diesel oil at 0.130 mg/l reduced growth by 50% in a two year experiment. No growth inhibition was noted at 0.03 mg/l and the plants recovered completely in oil free conditions. Coraliina officinalis, however, exhibited dramatic bleaching after the Sea Empress oil spill and died after the Torrey Canyon spill (Crump et al. 1999; Smith 1968). Encrusting corallines and Coraliina officinalis recovered from the Sea Empress spill quickly, bleaching only affecting the fronds or surface of crustose forms. Grazing gastropods, e.g. limpets are highly intolerant of oil spillage and if not killed are narcotinized and washed offshore and/or consumed by predators. The lower littoral populations are likely to be most vulnerable to oil spill and sublittoral fringe would be particularly affected at low tide. Although Alara esculenta may not be affected severely, the articulated coralline turf may be lost but recover quickly although the red algae may be intolerant. Grazers such as limpets, barnacles and meiofaunal crustaceans may also be lost from the community.

Not Assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Synthetic compound contamination [Show more]

Synthetic compound contamination

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

Evidence

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

Cole et al. 1999 suggest that macrophytes are generally intolerant of herbicides such as atrazine, simazine, diuron and linuron e.g. atrazine was lethal to Laminaria hyperborea sporophytes at 1mg/l and suppressed growth at 0.01 mg/l (Hopkin & Kain, 1978). Smith (1968) noted that Corallina officinalis was killed in areas of heavy spraying after the Torrey Canyon oil spill and affected at 6 m depth in areas of high wave action. High water specimens were more affected than low water specimens, presumably because they are emmersed for longer and had more contact with oil and dispersants. Gastropods are known to be highly sensitive to endocrine disrupters such as TBT. Crustaceans (e.g. amphipods, isopods, ostracods, copepods and barnacles) are also susceptible to endocrine disruption by synthetic chemicals. It is, therefore, likely that some taxa within IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes, especially grazing invertebrates and meiofauna will be intolerant of synthetic chemical contamination.

Not Assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Radionuclide contamination [Show more]

Radionuclide contamination

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

Evidence

No evidence

No evidence (NEv)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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No evidence (NEv)
NR
NR
NR
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Introduction of other substances [Show more]

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.

Not Assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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De-oxygenation [Show more]

De-oxygenation

Benchmark. Exposure to dissolved oxygen concentration of less than or equal to 2 mg/l for one week (a change from WFD poor status to bad status). Further detail

Evidence

Reduced oxygen concentrations have been shown to inhibit both photosynthesis and respiration in macroalgae (Kinne, 1977). Despite this, macroalgae are thought to buffer the environmental conditions of low oxygen, thereby acting as a refuge for organisms in oxygen depleted regions especially if the oxygen depletion is short-term (Frieder et al., 2012).  A rapid recovery from a state of low oxygen is expected if the conditions are transient, which is likely given the wave exposed distribution of defines IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes. 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). 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.

Sensitivity assessment.  Due to the mixing experienced in strongly wave exposed environments, resistance has been assessed as “High” resilience as “High”. Sensitivity has been assessed as “Not Sensitive” at the pressure benchmark level.

High
High
Medium
High
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High
High
High
High
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Not sensitive
High
Medium
High
Help
Nutrient enrichment [Show more]

Nutrient enrichment

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

Evidence

Organic enrichment is associated with eutrophication, increased siltation and turbidity (Fletcher 1996). Eutrophication is associated with loss of perennial algae and replacement by mussels or opportunistic algae (Fletcher 1996). Johnston & Roberts (2009) conducted a meta-analysis that reviewed 216 papers to assess how a variety of contaminants (including sewage and nutrient loading) affected 6 marine habitats (including intertidal and subtidal reefs). A 30-50% reduction in species diversity and richness was identified from all habitats exposed to the contaminant types. Johnston & Roberts (2009) also highlighted that macroalgal communities are relatively tolerant to contamination, but that metal and nutrient impacted intertidal communities can have low diversity assemblages which are dominated by opportunistic and fast growing species (Johnston & Roberts, 2009 and references therein). However due to the high wave exposure that defines IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes, it is likely that additional organic input to the system may be dispersed out of the biotope’s local vicinity (Johnston & Roberts, 2009). Increased nutrients may favour Mytilus edulis in IR.HIR.KFaR.Ala.Myt which may increase in cover and abundance. Corallina officinalis is also tolerant of polluted waters (Kindig & Littler, 1980).

Sensitivity assessment. IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes are however considered “Not Sensitive” at the benchmark level, which assumes compliance with good status as defined by the WFD.

Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Not sensitive
NR
NR
NR
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Organic enrichment [Show more]

Organic enrichment

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

Evidence

Organic enrichment is associated with eutrophication, increased siltation and turbidity (Fletcher 1996). Eutrophication is associated with loss of perennial algae and replacement by mussels or opportunistic algae (Fletcher 1996). Johnston & Roberts (2009) conducted a meta-analysis that reviewed 216 papers to assess how a variety of contaminants (including sewage and nutrient loading) affected six marine habitats (including intertidal and subtidal reefs).  A 30-50% reduction in species diversity and richness was identified from all habitats exposed to the contaminant types. Johnston & Roberts (2009) also highlighted that macroalgal communities are relatively tolerant to contamination, but that contaminated intertidal communities can have low diversity assemblages which are dominated by opportunistic and fast growing species (Johnston & Roberts, 2009 and references therein). Due to the high wave exposure that defines IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes, it is likely that additional organic input to the system may be dispersed out of the biotope’s local vicinity (Johnston & Roberts, 2009). Increased nutrients may favour Mytilus edulis in IR.HIR.KFaR.Ala.Myt which may increase in cover and abundance. Corallina officinalis is also tolerant of polluted waters (Kindig & Littler, 1980).

Sensitivity assessment. Resistance has been assessed as “Medium, (to represent potential changes in species diversity), resilience as “High. Sensitivity has been assessed as “Low”.

Medium
High
Medium
High
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High
High
Medium
High
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Low
High
Medium
High
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Physical Pressures

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ResistanceResilienceSensitivity
Physical loss (to land or freshwater habitat) [Show more]

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.

None
High
High
High
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Very Low
High
High
High
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High
High
High
High
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Physical change (to another seabed type) [Show more]

Physical change (to another seabed type)

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

Evidence

If rock substrata were replaced with sedimentary substrata this would represent a fundamental change in habitat type, which Alaria esculenta would not tolerate (Birkett et al., 1998). The biotope would be lost.

Sensitivity assessment. Resistance to the pressure is considered ’None‘, and resilience ’Very low‘ or ‘None’. The sensitivity of this biotope to change from hard rock or artificial substrata to sedimentary or soft rock substrata  is assessed as ’High’.

None
High
High
High
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Very Low
High
High
High
Help
High
High
High
High
Help
Physical change (to another sediment type) [Show more]

Physical change (to another sediment type)

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

Evidence

Not relevant to hard rock biotopes.

Not relevant (NR)
NR
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Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Habitat structure changes - removal of substratum (extraction) [Show more]

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

Not relevant to hard rock biotopes.

Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Abrasion / disturbance of the surface of the substratum or seabed [Show more]

Abrasion / disturbance of the surface of the substratum or seabed

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

Evidence

The sublittoral fringe is unlikely to be significantly impacted by trampling due to its position of the lower shore but may be prone to abrasion from moorings or low tide landings. Given its resilience to wave action Alaria esculenta is unlikely to be significantly damaged by abrasion although the understorey coralline turf may suffer some damage. The coralline turf meiofauna will probably be lost as a result of trampling. Moderate trampling on articulated coralline algal turf in the New Zealand intertidal (Brown & Taylor 1999; Schiel & Taylor 1999) resulted in reduced turf height, declines in turf densities, and loss of crustose bases in some case probably due to loss of the canopy algae and resultant desiccation. Calcification is thought to an adaptation to grazing and sediment scour (Littler & Kauker 1984).

If exposed to moorings, groundings, or passing fishing gear, the resultant abrasion may result in the physical removal of a proportion of the Alaria esculenta canopy. Depending on the scale of the impact, although no evidence of this impact was found.  However, Alaria esculenta has been shown to be an opportunistic colonizing species, capable of rapid recovery (see resilience section).

Sensitivity assessment. Resistance has been assessed as ’Medium‘, resilience as  ‘High‘. Sensitivity has been assessed as ’Low’.

Medium
Low
NR
NR
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High
High
Low
High
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Low
Low
NR
NR
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Penetration or disturbance of the substratum subsurface [Show more]

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

Not relevant to hard rock biotopes.

Not relevant (NR)
NR
NR
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Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
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Changes in suspended solids (water clarity) [Show more]

Changes in suspended solids (water clarity)

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

Evidence

Suspended Particle Matter (SPM) concentration has a linear relationship with sub surface light attenuation (Kd) (Devlin et al., 2008). Light penetration influences the maximum depth at which kelp species can grow and it has been reported that laminarians grow at depths at which the light levels are reduced to 1 percent of incident light at the surface. Maximal depth distribution of laminarians, therefore, varies from 100 m in the Mediterranean to only 6-7 m in the silt-laden German Bight. In European Atlantic waters, the depth limit is typically 35 m.

Alaria esculenta is not found in areas of siltation and sediment scour (Birkett et al. 1998). Increased siltation and sediment scour inhibits photosynthesis and algal growth, interfere with spore or larval recruitment plus smother germlings and gametophytes (Fletcher 1996). However, the high degree of wave exposure that typically defines IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes is likely to clear suspended sediments relatively quickly. If low water clarity is persistent and wave exposure decreased then low energy silted kelp biotopes (IR.LIR.K) may proliferate. Once siltation returns to its pre-effect level the biotope is likely to recover its canopy within a year and the rest of the community in no more than five years. Increased siltation will also increase turbidity. Increased sediment my benefit Mytilus edulis and its abundance may increase in IR.HIR.KFaR.Ala.Myt although large individuals are likely to be removed by wave action.

Increased turbidity is likely to reduce the depth to which Alaria  esculenta can grow. However, an increase of one level in WFD water clarity scale for a period of one year is unlikely to affect the population since Alaria esculenta’s lower limit, is generally determined by competition from other Laminarians rather than light penetration.

Sensitivity assessment. Resistance has been assessed as Medium, Resilience as High. Sensitivity has been assessed as Low.

Medium
Low
NR
NR
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High
High
Low
High
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Low
Low
Low
Low
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Smothering and siltation rate changes (light) [Show more]

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

Due to their size juvenile sporophytes, germlings, gametophytes and spores are likely to be inundated by deposition of 5 cm during a discrete event but the high wave exposure that defines the distribution of IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala (plus associated sub-biotopes deposited sediments) are likely to be removed rapidly and any effects of inundation are likely to be temporary.

Sensitivity assessment. Resistance has been assessed as ’High‘ and resilience as ’High‘. Sensitivity has been assessed as ’Not Sensitive‘.

High
Medium
Low
Medium
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High
High
High
High
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Not sensitive
Medium
Low
Medium
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Smothering and siltation rate changes (heavy) [Show more]

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

Due to their size juvenile sporophytes, germlings, gametophytes and spores are likely to be inundated by deposition of 30cm during a discrete event but the high wave exposure that defines the distribution of IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala (plus associated sub-biotopes deposited sediments) are likely to be removed rapidly and any effects of inundation are likely to be temporary.

Sensitivity assessment. Resistance has been assessed as ’High‘ and resilience as ’High‘. Sensitivity has been assessed as ’Not Sensitive‘.

High
Medium
Low
Medium
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High
High
High
High
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Not sensitive
Medium
Low
Medium
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Litter [Show more]

Litter

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

Evidence

Not assessed.

Not Assessed (NA)
NR
NR
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Not assessed (NA)
NR
NR
NR
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Not assessed (NA)
NR
NR
NR
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Electromagnetic changes [Show more]

Electromagnetic changes

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

Evidence

No evidence

No evidence (NEv)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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No evidence (NEv)
NR
NR
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Underwater noise changes [Show more]

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

Not relevant (NR)
NR
NR
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Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Introduction of light or shading [Show more]

Introduction of light or shading

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

Evidence

There was no evidence to suggest that anthropogenic light sources would affect IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes. Shading (e.g. by construction of a pontoon, pier etc) could adversely affect the biotope in areas where the water clarity is also low, and tip the balance to shade tolerant species, resulting in the loss of the biotope directly within the shaded area, or a reduction in laminarian abundance from forest to park type biotopes.

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

Low
Low
NR
NR
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High
High
High
High
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Low
Low
NR
NR
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Barrier to species movement [Show more]

Barrier to species movement

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

Evidence

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

Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Death or injury by collision [Show more]

Death or injury by collision

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

Evidence

Not relevant.  Collision from grounding vessels is addressed under abrasion above.

Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Visual disturbance [Show more]

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

Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Not relevant (NR)
NR
NR
NR
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Biological Pressures

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ResistanceResilienceSensitivity
Genetic modification & translocation of indigenous species [Show more]

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

No evidence (NEv)
NR
NR
NR
Help
Not relevant (NR)
NR
NR
NR
Help
No evidence (NEv)
NR
NR
NR
Help
Introduction or spread of invasive non-indigenous species [Show more]

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 and Sargassum muticum. Sargassum muticum is a circumglobal invasive species and is recorded 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. 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. It is a poor competitor under low light and only develops dense canopies in shallow areas (Engelen et al., 2015). In Limfjorden, Denmark between 1984 and 1997 (Staehr et al., 2000; Engelen et al., 2015; de Bettignies et al., 2021). 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 but wave exposure has been reported to restrict the growth and survival of Sargassum muticum (Staehr et al., 2000). 

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). It 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 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) and It is found predominantly in low intertidal to shallow subtidal habitats (Epstein et al., 2019b). 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 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 Laminaria hyperborea.  

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. 

Sensitivity assessment. This biotope (IR.HIR.KFaR.Ala.Myt) is extremely exposed to wave action and found within the sublittoral fringe with very strong to weak tidal streams. Sargassum muticum prefers wave sheltered shallow sites in the sublittoral fringe and shallow infralittoral. It was reported to out-compete and replace Saccharina latissima in the Limfjorden and achieve maximum abundance between 1 and 4 m (Staehr et al., 2000; Engelen et al., 2015). However, no evidence of the effects of Sargassum on Alaria esculenta beds was found. Therefore, as Alaria dominates the very exposed coasts it is unlikely that Sargassum will be able to survive within these conditions that characterize the biotope.  

Undaria pinnatifida has the potential to colonize and co-exist in refugia within Laminaria sp. dominated habitats that are within its shallow depth range (+ 1 to – 4 m) and sheltered from wave action. However, like Sargassum muticum, it is highly unlikely that Undaria pinnatifida will be able to colonize or survive within this biotope due to the extreme exposure to wave action that characterizes this biotope. Therefore, resistance to Sargassum or Undaria is assessed as ‘High’, resilience as 'High', and sensitivity is assessed as ‘Not Sensitive’. Overall, confidence is assessed as ‘Low’ due to evidence of variation and the site-specific nature of competition between native kelps and Undaria pinnatifida

High
Low
NR
NR
Help
High
High
High
High
Help
Not sensitive
Low
NR
NR
Help
Introduction of microbial pathogens [Show more]

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

Streblonema sp. is associated with spot disease in kelps and has been found growing on Alaria esculenta (Lein et al. 1991) but no incidence of Alaria esculenta spot disease was found. Corallina officinalis may host several epiphytes of which Titanoderma corallinae is thought to cause tissue damage. Hyperplasia or gall growths are often seen as dark spots on Laminaria digitata and have been associated with endophytic brown filamentous algae. There is no evidence in the literature that infection by microbial pathogens results in a mass death of kelp populations and the kelp themselves are known to regulate bacterial infections through iodine metabolism (Cosse et al., 2009).

Sensitivity assessment. Resistance has been assessed as ’High‘, resilience as ’High‘. Sensitivity has been assessed as ’Not sensitive’.

High
Medium
Medium
Low
Help
High
High
High
High
Help
Not sensitive
Medium
Medium
Low
Help
Removal of target species [Show more]

Removal of target species

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

Evidence

Alaria esculenta has recently received commercial interest as a consumable product called “Sea Vegetables” or “Atlantic Wakame Kelp”. However, no studies examining the effect of commercial extraction of Alaria esculenta biotopes were found. Removal of the algal canopy would expose the understorey fauna and flora to increased desiccation. Experimental macroalgal canopy removal experiments conducted in the Isle of Man (Hawkings & Harkin, 1985) found that following the removal of the macroalgal canopy the understorey encrusting red algae became bleached and died within a week. Mytilus edulis settlement has also been found significantly higher in close proximity to Alaria esculenta and is thought to increase beneath Alaria esculenta canopies (Bégin et al., 2004).  Therefore, any loss of Alaria esculenta, as a result of commercial extraction, may dramatically affect the understorey community.

Traditionally Laminaria digitata was added to agricultural lands as fertilizers; now Laminaria species are used in a range of different products, with its alginates used in the cosmetic, pharmaceutical and agri-food industries (Kervarec et al., 1999; McHugh, 2003). Laminaria digitata is harvested with a ‘Scoubidou’ (a curved iron hook which is mechanically operated) in France. This device is considered to be selective- only harvesting individuals older than 2 years (Arzel, 2002). France reportedly harvests 75,000t kelp, mainly consisting of Laminaria digitata annually (FAO, 2007). The loss of Laminaria digitata would represent as a significant change to IR.HIR.KFaR.Ala.Ldig.

Corallina officinalis is collected for medical purposes; the fronds are dried and converted to hydroxyapatite and used as bone forming material (Ewers et al. 1987). It is also sold as a powder for use in the cosmetic industry. Moderate trampling on articulated coralline algal turf in the New Zealand intertidal (Brown & Taylor 1999; Schiel & Taylor 1999) resulted in reduced turf height, declines in turf densities, and loss of crustose bases in some case probably due to loss of the canopy algae and resultant desiccation. Calcification is thought to be an adaptation to grazing and sediment scour (Littler & Kauker 1984). Corallina officinalis produces spores over a protracted period and can colonize artificial substratum within one week in the intertidal (Harkin & Lindbergh 1977; Littler & Kauker 1984). The crustose base enables Corallina officinalis to survive the loss of fronds.

Sensitivity assessment. There is little evidence for the effects of commercial harvesting of Alaria esculenta. If it is assumed that all canopy-forming kelp are removed then resistance would be assessed as ’None‘, resilience would be assessed as ’Medium‘. Sensitivity has been assessed as ’Medium‘. Within IR.HIR.KFaR.AlaAnCrSp and IR.HIR.KFaR.Ala.Myt, monospecific canopies of Alaria esculenta are expected to recover quicker than mixed canopies of Laminaria digitata (as in IR.HIR.KFaR.Ala.Ldig).

None
High
High
High
Help
Medium
High
High
High
Help
Medium
High
High
High
Help
Removal of non-target species [Show more]

Removal of non-target species

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

Evidence

Incidental/accidental removal of Alaria esculenta is likely to cause similar effects to that of direct harvesting; hence, the same evidence has been used for both pressure assessments.

Alaria esculenta has recently received commercial interest as a consumable product called “Sea Vegetables” or “Atlantic Wakame Kelp”. However, no studies examining the effect of commercial extraction of Alaria esculenta biotopes were found. Removal of the algal canopy would expose the understorey fauna and flora to increased desiccation. Experimental macroalgal canopy removal experiments conducted in the Isle of Man (Hawkings & Harkin, 1985) found that following the removal of the macroalgal canopy the understorey encrusting red algae became bleached and died within a week. Mytilus edulis settlement has also been found significantly higher in close proximity to Alaria esculenta and is thought to increase beneath Alaria esculenta canopies (Bégin et al., 2004).  Therefore, any loss of Alaria esculenta, as a result of commercial extraction, may dramatically affect the understorey community.

Traditionally Laminaria digitata was added to agricultural lands as fertilizers; now Laminaria species are used in a range of different products, with its alginates used in the cosmetic, pharmaceutical and agri-food industries (Kervarec et al., 1999; McHugh, 2003). Laminaria digitata is harvested with a ‘Scoubidou’ (a curved iron hook which is mechanically operated) in France. This device is considered to be selective- only harvesting individuals older than 2 years (Arzel, 2002). France reportedly harvests 75,000t kelp, mainly consisting of Laminaria digitata annually (FAO, 2007). The loss of Laminaria digitata would represent a significant change to IR.HIR.KFaR.Ala.Ldig.

Corallina officinalis is collected for medical purposes; the fronds are dried and converted to hydroxyapatite and used as bone forming material (Ewers et al. 1987). It is also sold as a powder for use in the cosmetic industry. Moderate trampling on articulated coralline algal turf in the New Zealand intertidal (Brown & Taylor 1999; Schiel & Taylor 1999) resulted in reduced turf height, declines in turf densities, and loss of crustose bases in some case probably due to loss of the canopy algae and resultant desiccation. Calcification is thought to be an adaptation to grazing and sediment scour (Littler & Kauker 1984). Corallina officinalis produces spores over a protracted period and can colonize artificial substratum within one week in the intertidal (Harkin & Lindbergh 1977; Littler & Kauker 1984). The crustose base enables Corallina officinalis to survive the loss of fronds.

Sensitivity assessment. There is little published evidence for the effects of commercial harvesting of Alaria esculenta. If it is assumed that all canopy forming kelp are removed then resistance would be assessed as ’None‘, resilience would be assessed as ’Medium‘. Sensitivity has been assessed as ’Medium‘. Within IR.HIR.KFaR.AlaAnCrSp and IR.HIR.KFaR.Ala.Myt, monospecific canopies of Alaria esculenta are expected to recover quicker than mixed canopies of Laminaria digitata (as in IR.HIR.KFaR.Ala.Ldig).

None
High
High
High
Help
Medium
High
High
High
Help
Medium
High
High
High
Help

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Citation

This review can be cited as:

Stamp, T.E., Williams, E., Tyler-Walters, H., & Burdett, E.G. 2023. Alaria esculenta, Mytilus edulis and coralline crusts on very exposed sublittoral fringe bedrock. In Tyler-Walters H. Marine Life Information Network: Biology and Sensitivity Key Information Reviews, [on-line]. Plymouth: Marine Biological Association of the United Kingdom. [cited 21-04-2024]. Available from: https://www.marlin.ac.uk/habitat/detail/217

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Last Updated: 31/10/2023

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