Alaria esculenta on exposed sublittoral fringe bedrock

Summary

UK and Ireland classification

Description

Exposed sublittoral fringe bedrock with an Alaria esculenta forest and an encrusting fauna of the mussel Mytilus edulis and barnacles such as Semibalanus balanoides. The kelp Laminaria digitata can be part of the canopy. Underneath the canopy are red seaweeds such as Mastocarpus stellatus and Palmaria palmata, while encrusting coralline red algae such as Lithothamnion graciale covers the rock surface. The limpet Patella vulgata can be found grazing the rock surface, while the whelk Nucella lapillus is preying on the limpets, barnacles and mussels. Two variants of this biotope are described. In more wave exposed conditions Laminaria digitata is absent and the rock surface is often characterised by dense patches of mussels (Ala.Myt). In slightly less exposed sites the Alaria esculenta is mixed with Laminaria digitata (Ala.Ldig). This biotope is found in the sublittoral fringe on exposed shores, typically occupying the extreme lower shore down to 1 or 2 m depth, although it can also extend down to 15 m depth on very exposed coasts. It is generally found below the mussel-barnacle zone of the lower shore (MytB) or a narrow band of the seaweed-dominated biotopes featuring dense Himanthalia elongata or red seaweeds (Him, Mas). Below the Alaria esculenta zone, the upper infralittoral rock generally supports a Laminaria hyperborea kelp community (LhypFa, LhypR.Ft or Lhyp.Ft). (Information taken from JNCC, 2022). 

Depth range

Lower shore, 0-5 m

Additional information

This review of IR.HIR.KFaR.Ala represents the sensitivity of the sub-biotope and similar biotopes IR.HIR.KFaR.Ala.Myt, IR.HIR.KFaR.Ala.Ldig, IR.HIR.KFaR.AlaAnCrSp.

Listed By

Habitat review

Ecology

Ecological and functional relationships

  • Alaria esculenta is able to out-compete other Laminarians in wave exposed sublittoral fringe due to its rapid growth rate and ability to withstand wave exposed conditions. It is particularly successful in exposed areas due to its flexible stipe and narrow, streamlined, blade.
  • Grazers are relatively rare in the sublittoral fringe and canopy interactions may be the most important structuring agency (Hawkins & Hartnoll 1985). The sweeping action of Laminaria digitata, and presumably, Alaria esculenta, in wave exposed conditions prevents colonization by ephemeral algae by abrasion (Hawkins & Hartnoll 1985).
  • The understorey is dominated by encrusting corallines and Corallina officinalis turf. In wave exposed sites the erect coralline turf grows very compactly reducing the interstitial space (exacerbated by the presence of small Mytilids) and affecting the interstitial fauna. Dommanses (1968) showed that the coralline turf fauna varied with wave exposure. Wave exposed sites were dominated by amphipods and short-legged isopods capable of grasping the fronds firmly. Interstitial fauna consists of grazers and suspension feeders (Dommaneses 1968) that probably remove ephemeral algae and epiphytes from Corallina officinalis.
  • On Rockall, the extreme wave exposure results in Alaria esculenta forest dominating both the sublittoral and infralittoral zone in the deeper areas. In the Rockall Alaria forest, the holdfasts of Alaria esculenta become covered in a thick layer of encrusting coralline algae and, after the death of the alga, the holdfast rots leaving a space under the coralline crust that is a habitat for several mobile species that would most likely not survive on the open rock in such a wave exposed situation (K. Hiscock, pers. Comm.).
  • Barnacle species are suspension feeders, that probably take algal spores and larvae that would otherwise settle within the community. Birkett et al. (1998b) point out that active suspension feeding by Mytilus edulis probably removes large numbers of settling algal spores and also compete for space. However, in the wave exposed sublittoral fringe, the small size of individual mytilids suggests that larger individuals are removed by wave action.
  • Patellids are active grazers, however, they lack the necessary enzymes to digest Laminarian tissue (Birkett et al., 1998b) and probably do not graze Alaria esculenta extensively. However, they probably graze other algae and are important in keeping coralline turf and encrusting corallines free of ephemeral algae. Grazing activity of patellids probably remove Alaria esculenta and other kelp germlings as the limpets pass over them; a bulldozing effect (T. Hill pers. Comm.).
  • may graze Alaria esculenta but prefers Laminaria digitata when present.
  • Chitons were reported to be an important controlling agency in Alaria sp. Populations allowing an otherwise weaker competitor to dominate in the north east Pacific (Paine 1980).

Seasonal and longer term change

Alaria esculenta is quite ephemeral in nature and will settle on bare surfaces, including mobile boulders and in deeper water than the infralittoral fringe. Alaria esculenta releases spores between November and March with new sporophytes appearing in early spring (Birkett et al.1998b). Growth of Alaria esculenta slows in June and July and the lamina becomes eroded and torn in the following months. In extremely wave exposed conditions, especially in winter months, the blade may be reduced to just the midrib. Similarly, in wave exposed areas Laminaria digitata is stunted and may be removed by storms and appears tattered in the winter months.

Habitat structure and complexity

Alaria esculenta dominates the sublittoral fringe in areas exposed to severe wave action or where water surges along the sides of gullies (Lewis, 1964). Such wave exposed shores are also characterized by pink encrusting and erect corallines, including Corallina officinalis. This biotope (EIR.Ala) can be divided into two sub-biotopes depending on the degree of wave exposure EIR.Ala.Myt and EIR.Ala.Ldig. Alaria esculenta support few epizoics (e.g. Audouinella alariae on older specimens) and holdfasts yield few species (Lewis 1964; Birkett et al. 1998b). In areas of extreme wave exposure, on steeply sloping rock, exposed to oceanic swell EIR.Ala may extend up to 3 m above and below chart datum (Hiscock 1983).
In EIR.Ala.Myt

As the wave exposure decreases the width of the Alaria esculenta zone narrows and Laminaria digitata is able to invade the sublittoral fringe resulting in a mixed macroalgal stand and increased species richness, characteristic of EIR.Ala.Ldig.

EIR.Ala.Ldig usually occurs above Laminaria hyperborea forest although a narrow zone of Laminaria digitata (MIR.Ldig) may intervene. EIR.Ala.Ldig biotopes probably represent an intermediate community between very wave exposed shores dominated by EIR.Ala.Myt and more wave sheltered shores dominated by MIR.Ldig. On the extremely wave exposed steep and vertical rock faces of Rockall Alaria esculenta replaces Laminaria hyperboreaas the dominant kelp and extends to down to 35m in depth. Above 13m the biotope resembles EIR.Ala.Myt. However, from 14 - 35 m the understorey is covered by a dense turf of anemones and encrusting sponges. Cryptopleura ramosa dominates horizontal surfaces. Between 30 -35 m the Alaria esculenta thins and the rock surface bears a dense red algal turf.

Productivity

Kelp biotopes are highly productive and contribute up to 90 percent of their primary productivity to the detrital food webs of coastal areas in the form of drift algae, particulate and dissolved organic matter. For example primary productivity of Laminaria hyperborea kelp beds were estimated at 1225 gC/sq. meter/year (Mann 1982 cited in Raffaelli & Hawkins 1999). However, no estimates were found for Alaria esculenta biotopes, though figures are likely to be similar for all kelps (Tim Hill pers. comm.).

Recruitment processes

Laminarians, such as Alaria esculenta, exhibit alternation of generations. The sporophytes release meiotic haploid spores from sori located on sporophylls (born at the top of the short stipe) between November and March. Laminarian spores need to settle at high density so that the resultant gametophytes are close enough to cross fertilize. Laminarians produce vast numbers of spores and are expected to disperse over considerable distances. However, Sundene (1962) noted that germlings colonized within 10 m of adults in a Norwegian fjord, and Norton (1992) suggested that Alaria esculenta would exhibit less dispersal than other kelp species due to the basal location of the sporophylls. Experiments on algal re-colonization in kelp beds (Kain 1975; Hawkins & Harkin 1985; Hill 1993) show that Alaria esculenta is an opportunistic colonizing species, appearing early in the algal succession (c. 3 months after clearance of dominant algae; especially in areas cleared in the winter months) before being out-competed by other kelp species (on moderately exposed shores). 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 extreme 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 1989) 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 (e.g. Patella pellucida).

Time for community to reach maturity

Alaria esculenta is an opportunistic and rapidly colonizing species (see above) capable of growing 20 cm/month in optimal conditions. 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). 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.

Additional information

Little information on the sublittoral fringe communities was available. Therefore, the material presented is based on the general ecology of the key and important characterizing species.

Preferences & Distribution

Habitat preferences

Depth Range Lower shore, 0-5 m
Water clarity preferences
Limiting Nutrients Nitrogen (nitrates), Phosphorus (phosphates)
Salinity preferences Full (30-40 psu)
Physiographic preferences Open coast
Biological zone preferences Sublittoral fringe
Substratum/habitat preferences Bedrock, Large to very large boulders
Tidal strength preferences Moderately strong 1 to 3 knots (0.5-1.5 m/sec.), Weak < 1 knot (<0.5 m/sec.)
Wave exposure preferences Exposed, Extremely exposed, Very exposed
Other preferences No text entered.

Additional Information

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Species composition

Species found especially in this biotope

    Rare or scarce species associated with this biotope

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    Additional information

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    Sensitivity review

    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 & 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., 1998b). Alaria esculenta has a compact holdfast, a flexible “short” stipe and a flexible frond with a conspicuous reinforcing midrib (Birkett et al., 1998). 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 the 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 4m (Werner & Kraan, 2004), fronds can reach a total length of 2m, however, growth rates are locally variable and are more typically 30-90 cm 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 (Fredersorf 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), and observed that Alaria esculenta germlings were restricted to within 10 m of the parental source in an Alaria esculenta translocation experiment conducted in a Norwegian fjord.

    Alaria esculenta is an opportunistic colonizing species (Kain 1975; 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 out-competed 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 (1975) conducted a similar experiment to Hawkins & Harkin (1985), however over a longer time period (>2 years).  Laminaria digitata was cleared from moderately wave exposed concrete blocks at Port Erin, Isle of Man, and the subsequent “succession” of algae communities was documented. Following clearance Laminaria digitata was considered re-established two years after removal, while the understorey red seaweed species returned one year later. Engelen (2010) observed a similar recovery time in Britany, France.  Patches of Laminaria digitata (0.25m2 ) were removed.. Laminaria digitata returned to conditions prior to removal within 18-24 months, although competition for space by Saccorhiza polyschides reduced recovery rates in the first year of recolonization. Engelen (2010) stated that Laminaria digitata forest recovery rates varied between seasons, with autumn recovery being more rapid than spring (taking a minimum of 12 months).

    The dispersal of Laminaria digitata’s spores and subsequent successful recruitment has been recorded 600 m from reproductive individuals (Chapman, 1981). The growth rate of Laminaria digitata changes with the seasons. Growth is rapid from February to July, slower in August to January, and occurs diffusely in the Lamina (blade; Kain, 1979). Zoospores are produced at temperatures lower than 18°C with a minimum of 10 weeks a year between 5-18°C needed to ensure spore formation (Bartsch, 2013).  Thus, temperature and by default season impacts the level of reproductive activity. Furthermore, experimental clearance experiments of Laminaria digitata (Kain 1975; Hawkins & Harkin 1985; Hill 1993; Engelen, 2010) found that following clearance Laminaria digitata re-colonization takes 12-24 months. Interspecific competition from ephemeral algae was also found to slow recovery times (Engelen, 2010).

    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 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 1989) 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). 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. Therefore general resilience of IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes has been assessed as High. 

    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.

    Hydrological Pressures

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    ResistanceResilienceSensitivity
    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 macroalga 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 temperatures 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) (Birket et al., 1998), 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 2/5°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
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    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’snorthern range edge (Svalbard) it is a prominent macro-algae on sub-littoral 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 temperatures 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) (Birket et al., 1998), 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
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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 exposures 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
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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
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    High
    High
    Low
    High
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    Low
    Low
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    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
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    High
    High
    Low
    High
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    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
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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)
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    Not assessed (NA)
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    Not assessed (NA)
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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 2 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
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    Not assessed (NA)
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    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
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    Not assessed (NA)
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    Not assessed (NA)
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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
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    Not relevant (NR)
    NR
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    No evidence (NEv)
    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)
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    Not assessed (NA)
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    Not assessed (NA)
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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 environment, 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
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    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 relative

    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
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    High
    High
    Medium
    High
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    Low
    High
    Medium
    High
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    Physical Pressures

    Use [show more] / [show less] to open/close text displayed

    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
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    High
    High
    High
    High
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    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)
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    Not relevant (NR)
    NR
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    Not relevant (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)
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    Not relevant (NR)
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    Not relevant (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
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    High
    High
    Low
    High
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    Low
    Low
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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)
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    Not relevant (NR)
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    Not relevant (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 may 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
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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
    High
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    High
    High
    High
    High
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    Not sensitive
    Medium
    Low
    High
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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 30 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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    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. No evidence to suggest that litter would affect IR.HIR.KFaR.AlaAnCrSp & IR.HIR.KFaR.Ala plus associated sub-biotopes was found.

    Not Assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    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
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    No evidence (NEv)
    NR
    NR
    NR
    Help
    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
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    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
    Help
    High
    High
    High
    High
    Help
    Low
    Low
    NR
    NR
    Help
    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 and propagules.  But spore or propagule dispersal is not considered under the pressure definition and benchmark.

    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    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
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    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
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help

    Biological Pressures

    Use [show more] / [show less] to open/close text displayed

    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

    Not relevant (NR)
    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) 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 Alarias 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 the 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 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) Sensitivity of the latter would be assessed as follows; resistance ’None‘, resilience as ’High‘, Sensitivity as ’Medium’.

    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 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 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) Sensitivity of the latter would be assessed as follows; resistance ’None‘, resilience as ’High‘, Sensitivity as ’Medium’.

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

    Bibliography

    1. Andrew, N.L. & Viejo, R.M., 1998. Ecological limits to the invasion of Sargassum muticum in northern Spain. Aquatic Botany, 60 (3), 251-263. DOI https://doi.org/10.1016/S0304-3770(97)00088-0

    2. Arnold, M., Teagle, H., Brown, M.P. & Smale, D.A., 2016. The structure of biogenic habitat and epibiotic assemblages associated with the global invasive kelp Undaria pinnatifida in comparison to native macroalgae. Biological Invasions, 18 (3), 661-676. DOI https://doi.org/10.1007/s10530-015-1037-6

    3. Arzel, P., 2002. La laminaire digitée. Les nouvelles de l’Ifremer, 33 (4).

    4. Arzel, P., 1998. Les laminaires sur les côtes bretonnes. Évolution de l'exploitation et de la flottille de pêche, état actuel et perspectives. Plouzané, France: Ifremer.

    5. Bamber, R.N. & Irving, P.W., 1993. The Corallina run-offs of Bridgewater Bay. Porcupine Newsletter, 5, 190-197.

    6. Bartsch, I., Vogt, J., Pehlke, C. & Hanelt, D., 2013. Prevailing sea surface temperatures inhibit summer reproduction of the kelp Laminaria digitata at Helgoland (North Sea). Journal of Phycology, 49 (6), 1061-1073.

    7. Beszczynska-Möller, A., & Dye, S.R., 2013. ICES Report on Ocean Climate 2012. In ICES Cooperative Research Report, vol. 321 pp. 73.

    8. Birkett, D.A., Maggs, C.A., Dring, M.J. & Boaden, P.J.S., 1998b. Infralittoral reef biotopes with kelp species: an overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Natura 2000 report prepared by Scottish Association of Marine Science (SAMS) for the UK Marine SACs Project., Scottish Association for Marine Science. (UK Marine SACs Project, vol VI.), 174 pp. Available from: http://ukmpa.marinebiodiversity.org/uk_sacs/pdfs/reefkelp.pdf

    9. Bower, S.M., 1996. Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Bald-sea-urchin Disease. [On-line]. Fisheries and Oceans Canada. [cited 26/01/16]. Available from: http://www.dfo-mpo.gc.ca/science/aah-saa/diseases-maladies/bsudsu-eng.html

    10. Britton-Simmons, K.H., 2004. Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Marine Ecology Progress Series, 277, 61-78. DOI https://doi.org/10.3354/meps277061

    11. Brodie J., Williamson, C.J., Smale, D.A., Kamenos, N.A., Mieszkowska, N., Santos, R., Cunliffe, M., Steinke, M., Yesson, C. & Anderson, K.M., 2014. The future of the northeast Atlantic benthic flora in a high CO2 world. Ecology and Evolution, 4 (13), 2787-2798. DOI  https://doi.org/10.1002/ece3.1105

    12. Brown, P.J. & Taylor, R.B., 1999. Effects of trampling by humans on animals inhabiting coralline algal turf in the rocky intertidal. Journal of Experimental Marine Biology and Ecology, 235, 45-53.

    13. Bryan, G.W., 1984. Pollution due to heavy metals and their compounds. In Marine Ecology: A Comprehensive, Integrated Treatise on Life in the Oceans and Coastal Waters, vol. 5. Ocean Management, part 3, (ed. O. Kinne), pp.1289-1431. New York: John Wiley & Sons.

    14. Burrows, M.T., Smale, D., O’Connor, N., Rein, H.V. & Moore, P., 2014. Marine Strategy Framework Directive Indicators for UK Kelp Habitats Part 1: Developing proposals for potential indicators. Joint Nature Conservation Comittee,  Peterborough. Report no. 525.

    15. Casas, G., Scrosati, R. & Piriz, M.L., 2004. The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biological Invasions, 6 (4), 411-416.

    16. Castric-Fey, A., Girard, A. & L'Hardy-Halos, M.T., 1993. The Distribution of Undaria pinnatifida (Phaeophyceae, Laminariales) on the Coast of St. Malo (Brittany, France). Botanica Marina, 36 (4), 351-358. DOI https://doi.org/10.1515/botm.1993.36.4.351

    17. Chapman, A.R.O., 1981. Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St. Margaret's Bay, Eastern Canada. Marine Biology, 62, 307-311.

    18. Christie, H., Fredriksen, S. & Rinde, E., 1998. Regrowth of kelp and colonization of epiphyte and fauna community after kelp trawling at the coast of Norway. Hydrobiologia, 375/376, 49-58.

    19. Cole, S., Codling, I.D., Parr, W. & Zabel, T., 1999. Guidelines for managing water quality impacts within UK European Marine sites. Natura 2000 report prepared for the UK Marine SACs Project. 441 pp., Swindon: Water Research Council on behalf of EN, SNH, CCW, JNCC, SAMS and EHS. [UK Marine SACs Project.]. Available from: http://ukmpa.marinebiodiversity.org/uk_sacs/pdfs/water_quality.pdf

    20. Connor, D.W., Dalkin, M.J., Hill, T.O., Holt, R.H.F. & Sanderson, W.G., 1997a. Marine biotope classification for Britain and Ireland. Vol. 2. Sublittoral biotopes. Joint Nature Conservation Committee, Peterborough, JNCC Report no. 230, Version 97.06., Joint Nature Conservation Committee, Peterborough, JNCC Report no. 230, Version 97.06.

    21. Crisp, D.J. & Mwaiseje, B., 1989. Diversity in intertidal communities with special reference to the Corallina officinalis community. Scientia Marina, 53, 365-372.

    22. Crump, R.G., Morley, H.S., & Williams, A.D., 1999. West Angle Bay, a case study. Littoral monitoring of permanent quadrats before and after the Sea Empress oil spill. Field Studies, 9, 497-511.

    23. Dauvin, J.C., Bellan, G., Bellan-Santini, D., Castric, A., Francour, P., Gentil, F., Girard, A., Gofas, S., Mahe, C., Noel, P., & Reviers, B. de., 1994. Typologie des ZNIEFF-Mer. Liste des parametres et des biocoenoses des cotes francaises metropolitaines. 2nd ed. Secretariat Faune-Flore, Museum National d'Histoire Naturelle, Paris (Collection Patrimoines Naturels, Serie Patrimoine Ecologique, No. 12). Coll. Patrimoines Naturels, vol. 12, Secretariat Faune-Flore, Paris.

    24. Davies, C.E. & Moss, D., 1998. European Union Nature Information System (EUNIS) Habitat Classification. Report to European Topic Centre on Nature Conservation from the Institute of Terrestrial Ecology, Monks Wood, Cambridgeshire. [Final draft with further revisions to marine habitats.], Brussels: European Environment Agency.

    25. Dayton, P.K., Tegner, M.J., Parnell, P.E. & Edwards, P.B., 1992. Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecological Monographs, 62, 421-445.

    26. De Bettignies, T., de Bettignies, F., Bartsch, I., Bekkby, T., Boiffin, A., Casado de Amezúa, P., Christie, H., Edwards, H., Fournier, N., García, A., Gauthier, L., Gillham, K., Halling, C., Harrald, M., Hennicke, J., Hernández, S., Kilnäs, M., Martinez, B., Mieszkowska, N., Moore, P., Moy, F., Mueller, M., Norderhaug, K.M., Ó Cadhla, O., Parry, M., Ramsay, K., Robertson, M., Russel, T., Serrão, E., Smale, D., Sousa Pinto, I., Steen, H., Street, M., Walday, M., Werner, T. & La Rivière, M., 2021. Background Document for Kelp Forests. OSPAR Commission, London, OSPAR 788/2021, 66 pp. Available from: https://www.ospar.org/documents?v=46796

    27. De Leij, R., Epstein, G., Brown, M.P. & Smale, D.A., 2017. The influence of native macroalgal canopies on the distribution and abundance of the non-native kelp Undaria pinnatifida in natural reef habitats. Marine Biology, 164 (7). DOI https://doi.org/10.1007/s00227-017-3183-0

    28. Devlin, M.J., Barry, J., Mills, D.K., Gowen, R.J., Foden, J., Sivyer, D. & Tett, P., 2008. Relationships between suspended particulate material, light attenuation and Secchi depth in UK marine waters. Estuarine, Coastal and Shelf Science, 79 (3), 429-439.

    29. Dieck, T.I., 1992. North Pacific and North Atlantic digitate Laminaria species (Phaeophyta): hybridization experiments and temperature responses. Phycologia, 31, 147-163.

    30. Dieck, T.I., 1993. Temperature tolerance and survival in darkness of kelp gametophytes (Laminariales: Phaeophyta) - ecological and biogeographical implications. Marine Ecology Progress Series, 100, 253-264.

    31. Dommasnes, A., 1968. Variation in the meiofauna of Corallina officinalis with wave exposure. Sarsia, 34, 117-124.

    32. Eckman, J.E. & Duggins, D.O., 1991. Life and death beneath macrophyte canopies: effects of understory kelps on growth rates and survival of marine, benthic suspension feeders. Oecologia, 87, 473-487.

    33. Edwards, A., 1980. Ecological studies of the kelp Laminaria hyperborea and its associated fauna in south-west Ireland. Ophelia, 9, 47-60.

    34. Elner, R.W. & Vadas, R.L., 1990. Inference in ecology: the sea urchin phenomenon in the northwest Atlantic. American Naturalist, 136, 108-125.

    35. Engelen, A.H., Serebryakova, A., Ang, P., Britton-Simmons, K., Mineur, F., Pedersen, M. F., & Toth, G., 2015. Circumglobal invasion by the brown seaweed Sargassum muticum. Oceanography and Marine Biology: An Annual Review, 53, 81-126.

    36. Epstein, G. & Smale, D.A., 2017. Undaria pinnatifida: A case study to highlight challenges in marine invasion ecology and management. Ecology and Evolution, 7 (20), 8624-8642. DOI https://doi.org/10.1002/ece3.3430

    37. Epstein, G. & Smale, D.A., 2018. Environmental and ecological factors influencing the spillover of the non-native kelp, Undaria pinnatifida, from marinas into natural rocky reef communities. Biological Invasions, 20 (4), 1049-1072. DOI https://doi.org/10.1007/s10530-017-1610-2

    38. Epstein, G., Foggo, A. & Smale, D.A., 2019a. Inconspicuous impacts: Widespread marine invader causes subtle but significant changes in native macroalgal assemblages. Ecosphere, 10 (7). DOI https://doi.org/10.1002/ecs2.2814

    39. Epstein, G., Hawkins, S.J. & Smale, D.A., 2019b. Identifying niche and fitness dissimilarities in invaded marine macroalgal canopies within the context of contemporary coexistence theory. Scientific Reports, 9. DOI https://doi.org/10.1038/s41598-019-45388-5

    40. Erwin, D.G., Picton, B.E., Connor, D.W., Howson, C.M., Gilleece, P. & Bogues, M.J., 1990. Inshore Marine Life of Northern Ireland. Report of a survey carried out by the diving team of the Botany and Zoology Department of the Ulster Museum in fulfilment of a contract with Conservation Branch of the Department of the Environment (N.I.)., Ulster Museum, Belfast: HMSO.

    41. Ewers, R., Kasperk, C. & Simmons, B., 1987. Biologishes Knochenimplantat aus Meeresalgen. Zahnaerztliche Praxis, 38, 318-320.

    42. FAO (Food and Agriculture Organization of the United Nations), 2007. Aquaculture production: values 1984-2005. FISHSTAT Plus - Universal software for fishery statistical time series [online or CD-ROM]. Fishery Information, Data and Statistics Unit. Food and Agriculture Organization of the United Nations, Rome, Italy.

    43. Farrell, P. & Fletcher, R., 2006. An investigation of dispersal of the introduced brown alga Undaria pinnatifida (Harvey) Suringar and its competition with some species on the man-made structures of Torquay Marina (Devon, UK). Journal of Experimental Marine Biology and Ecology, 334 (2), 236-243.

    44. Fletcher, R. & Farrell, P., 1998. Introduced brown algae in the North East Atlantic, with particular respect to Undaria pinnatifida (Harvey) Suringar. Helgolander Meeresuntersuchungen, 52 (3-4), 259-275.

    45. Fletcher, R.L., 1996. The occurrence of 'green tides' - a review. In Marine Benthic Vegetation. Recent changes and the Effects of Eutrophication (ed. W. Schramm & P.H. Nienhuis). Berlin Heidelberg: Springer-Verlag. [Ecological Studies, vol. 123].

    46. Fredersdorf, J., Müller, R., Becker, S., Wiencke, C. & Bischof, K., 2009. Interactive effects of radiation, temperature and salinity on different life history stages of the Arctic kelp Alaria esculenta (Phaeophyceae). Oecologia, 160 (3), 483-492.

    47. Fredriksen, S., Sjøtun, K., Lein, T.E. & Rueness, J., 1995. Spore dispersal in Laminaria hyperborea (Laminariales, Phaeophyceae). Sarsia, 80 (1), 47-53.

    48. Frieder, C., Nam, S., Martz, T. & Levin, L., 2012. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences, 9 (10), 3917-3930.

    49. Gommez, J.L.C. & Miguez-Rodriguez, L.J., 1999. Effects of oil pollution on skeleton and tissues of Echinus esculentus L. 1758 (Echinodermata, Echinoidea) in a population of A Coruna Bay, Galicia, Spain. In Echinoderm Research 1998. Proceedings of the Fifth European Conference on Echinoderms, Milan, 7-12 September 1998, (ed. M.D.C. Carnevali & F. Bonasoro) pp. 439-447. Rotterdam: A.A. Balkema.

    50. Gorman, D., Bajjouk, T., Populus, J., Vasquez, M. & Ehrhold, A., 2013. Modeling kelp forest distribution and biomass along temperate rocky coastlines. Marine Biology, 160 (2), 309-325.

    51. Grahame, J., & Hanna, F.S., 1989. Factors affecting the distribution of the epiphytic fauna of Corallina officinalis (L.) on an exposed rocky shore. Ophelia, 30, 113-129.

    52. Grandy, N., 1984. The effects of oil and dispersants on subtidal red algae. Ph.D. Thesis. University of Liverpool.

    53. Guiry, M.D. & Blunden, G., 1991. Seaweed Resources in Europe: Uses and Potential. Chicester: John Wiley & Sons.

    54. Hammer, L., 1972. Anaerobiosis in marine algae and marine phanerograms. In Proceedings of the Seventh International Seaweed Symposium, Sapporo, Japan, August 8-12, 1971 (ed. K. Nisizawa, S. Arasaki, Chihara, M., Hirose, H., Nakamura V., Tsuchiya, Y.), pp. 414-419. Tokyo: Tokyo University Press.

    55. Harkin, E., 1981. Fluctuations in epiphyte biomass following Laminaria hyperborea canopy removal. In Proceedings of the Xth International Seaweed Symposium, Gø teborg, 11-15 August 1980 (ed. T. Levring), pp.303-308. Berlin: Walter de Gruyter.

    56. Harlin, M.M., & Lindbergh, J.M., 1977. Selection of substrata by seaweed: optimal surface relief. Marine Biology, 40, 33-40.

    57. Hawkins, S.J. & Harkin, E., 1985. Preliminary canopy removal experiments in algal dominated communities low on the shore and in the shallow subtidal on the Isle of Man. Botanica Marina, 28, 223-30.

    58. Hawkins, S.J. & Hartnoll, R.G., 1985. Factors determining the upper limits of intertidal canopy-forming algae. Marine Ecology Progress Series, 20, 265-271.

    59. Hayward, P.J. 1988. Animals on seaweed. Richmond, Surrey: Richmond Publishing Co. Ltd. [Naturalists Handbooks 9].

    60. Heiser, S., Hall-Spencer, J.M. & Hiscock, K., 2014. Assessing the extent of establishment of Undaria pinnatifida in Plymouth Sound Special Area of Conservation, UK. Marine Biodiversity Records, 7, e93.

    61. Hill, T., 1993. Algal zonation in the sublittoral fringe: the importance of competition. Ph.D. Thesis., University of Liverpool, Liverpool, UK.

    62. Hiscock, K. & Mitchell, R., 1980. The Description and Classification of Sublittoral Epibenthic Ecosystems. In The Shore Environment, Vol. 2, Ecosystems, (ed. J.H. Price, D.E.G. Irvine, & W.F. Farnham), 323-370. London and New York: Academic Press. [Systematics Association Special Volume no. 17(b)].

    63. Hiscock, K., 1983. Water movement. In Sublittoral ecology. The ecology of shallow sublittoral benthos (ed. R. Earll & D.G. Erwin), pp. 58-96. Oxford: Clarendon Press.

    64. Holt, T.J., Jones, D.R., Hawkins, S.J. & Hartnoll, R.G., 1995. The sensitivity of marine communities to man induced change - a scoping report. Countryside Council for Wales, Bangor, Contract Science Report, no. 65.

    65. Hopkin, R. & Kain, J.M., 1978. The effects of some pollutants on the survival, growth and respiration of Laminaria hyperborea. Estuarine and Coastal Marine Science, 7, 531-553.

    66. Hull, S., 1997. Seasonal changes in diversity and abundance of ostracodes on four species of intertidal algae with differing structural complexity. Marine Ecology Progress Series, 161, 71-82.

    67. JNCC (Joint Nature Conservation Committee), 2022.  The Marine Habitat Classification for Britain and Ireland Version 22.04. [Date accessed]. Available from: https://mhc.jncc.gov.uk/

    68. JNCC (Joint Nature Conservation Committee), 2022.  The Marine Habitat Classification for Britain and Ireland Version 22.04. [Date accessed]. Available from: https://mhc.jncc.gov.uk/

    69. JNCC (Joint Nature Conservation Committee), 1999. Marine Environment Resource Mapping And Information Database (MERMAID): Marine Nature Conservation Review Survey Database. [on-line] http://www.jncc.gov.uk/mermaid

    70. Johnston, E.L. & Roberts, D.A., 2009. Contaminants reduce the richness and evenness of marine communities: a review and meta-analysis. Environmental Pollution, 157 (6), 1745-1752.

    71. Jones, C.G., Lawton, J.H. & Shackak, M., 1994. Organisms as ecosystem engineers. Oikos, 69, 373-386.

    72. Jones, D.J., 1971. Ecological studies on macro-invertebrate communities associated with polluted kelp forest in the North Sea. Helgolander Wissenschaftliche Meersuntersuchungen, 22, 417-431.

    73. Jones, L.A., Hiscock, K. & Connor, D.W., 2000. Marine habitat reviews. A summary of ecological requirements and sensitivity characteristics for the conservation and management of marine SACs. Joint Nature Conservation Committee, Peterborough. (UK Marine SACs Project report.). Available from: http://ukmpa.marinebiodiversity.org/uk_sacs/pdfs/marine-habitats-review.pdf

    74. Jones, N.S. & Kain, J.M., 1967. Subtidal algal recolonisation following removal of Echinus. Helgolander Wissenschaftliche Meeresuntersuchungen, 15, 460-466.

    75. Kain, J.M., 1964. Aspects of the biology of Laminaria hyperborea III. Survival and growth of gametophytes. Journal of the Marine Biological Association of the United Kingdom, 44 (2), 415-433.

    76. Kain, J.M. & Svendsen, P., 1969. A note on the behaviour of Patina pellucida in Britain and Norway. Sarsia, 38, 25-30.

    77. Kain, J.M., 1971a. Synopsis of biological data on Laminaria hyperborea. FAO Fisheries Synopsis, no. 87.

    78. Kain, J.M., 1975a. Algal recolonization of some cleared subtidal areas. Journal of Ecology, 63, 739-765.

    79. Kain, J.M., 1979. A view of the genus Laminaria. Oceanography and Marine Biology: an Annual Review, 17, 101-161.

    80. Kain, J.M., 1987. Photoperiod and temperature as triggers in the seasonality of Delesseria sanguinea. Helgolander Meeresuntersuchungen, 41, 355-370.

    81. Kain, J.M., & Norton, T.A., 1990. Marine Ecology. In Biology of the Red Algae, (ed. K.M. Cole & Sheath, R.G.). Cambridge: Cambridge University Press.

    82. Kain, J.M., Drew, E.A. & Jupp, B.P., 1975. Light and the ecology of Laminaria hyperborea II. In Proceedings of the Sixteenth Symposium of the British Ecological Society, 26-28 March 1974. Light as an Ecological Factor: II (ed. G.C. Evans, R. Bainbridge & O. Rackham), pp. 63-92. Oxford: Blackwell Scientific Publications.

    83. Karsten, U., 2007. Research note: salinity tolerance of Arctic kelps from Spitsbergen. Phycological Research, 55 (4), 257-262.

    84. Kervarec, F., Arzel, P. & Guyader, O., 1999. Fisher Behaviour and Economic Interactions Between Fisheries: Examining Seaweed and Scallop Fisheries of the Brest District (Western Brittany, France). The XIth Annual Conference of the European Association of Fisheries Economists. 6th-10th April 1999, Dublin, pp.

    85. Kindig, A.C., & Littler, M.M., 1980. Growth and primary productivity of marine macrophytes exposed to domestic sewage effluents. Marine Environmental Research, 3, 81-100.

    86. Kinne, O. (ed.), 1971a. Marine Ecology: A Comprehensive, Integrated Treatise on Life in Oceans and Coastal Waters. Vol. 1 Environmental Factors, Part 2. Chichester: John Wiley & Sons.

    87. Kinne, O., 1977. International Helgoland Symposium "Ecosystem research": summary, conclusions and closing. Helgoländer Wissenschaftliche Meeresuntersuchungen, 30(1-4), 709-727.

    88. Kitching, J., 1941. Studies in sublittoral ecology III. Laminaria forest on the west coast of Scotland; a study of zonation in relation to wave action and illumination. The Biological Bulletin, 80 (3), 324-337

    89. Kraan, S., 2017. Undaria marching on; late arrival in the Republic of Ireland. Journal of Applied Phycology, 29 (2), 1107-1114. DOI https://doi.org/10.1007/s10811-016-0985-2

    90. Kregting, L., Blight, A., Elsäßer, B. & Savidge, G., 2013. The influence of water motion on the growth rate of the kelp Laminaria hyperborea. Journal of Experimental Marine Biology and Ecology, 448, 337-345.

    91. Kruuk, H., Wansink, D. & Moorhouse, A., 1990. Feeding patches and diving success of otters, Lutra lutra, in Shetland. Oikos, 57, 68-72.

    92. Lang, C. & Mann, K., 1976. Changes in sea urchin populations after the destruction of kelp beds. Marine Biology, 36 (4), 321-326.

    93. Lein, T.E., Sjøtun, K. & Wakili, S., 1991. Mass-occurrence of a brown filamentous endophyte in the lamina of the kelp Laminaria hyperborea (Gunnerus) Foslie along the southwestern coast of Norway. Sarsia, 76 (3), 187-193. DOI https://doi.org/10.1080/00364827.1991.10413474

    94. Leinaas, H.P. & Christie, H., 1996. Effects of removing sea urchins (Strongylocentrotus droebachiensis): stability of the barren state and succession of kelp forest recovery in the east Atlantic. Oecologia, 105(4), 524-536.

    95. Lewis, J.R., 1964. The Ecology of Rocky Shores. London: English Universities Press.

    96. Littler, M.M., & Kauker, B.J., 1984. Heterotrichy and survival strategies in the red alga Corallina officinalis L. Botanica Marina, 27, 37-44.

    97. Lobban, C.S. & Harrison, P.J., 1997. Seaweed ecology and physiology. Cambridge: Cambridge University Press.

    98. Lüning, K., 1990. Seaweeds: their environment, biogeography, and ecophysiology: John Wiley & Sons.

    99. Macleod, A., Cottier-Cook, E., Hughes, D. & Allen, C., 2016. Investigating the impacts of marine invasive non-native species. Natural England Commissioned Report NECR223, Natural England, 58 pp. Available from: https://pureadmin.uhi.ac.uk/ws/portalfiles/portal/3729569/NECR223_edition_1.pdf

    100. Mann, K.H., 1982. Kelp, sea urchins, and predators: a review of strong interactions in rocky subtidal systems of eastern Canada, 1970-1980. Netherlands Journal of Sea Research, 16, 414-423.

    101. Miller III, H.L., Neale, P.J. & Dunton, K.H., 2009. Biological weighting functions for UV inhibtion of photosynthesis in the kelp Laminaria hyperborea (Phaeophyceae) 1. Journal of Phycology, 45 (3), 571-584.

    102. Minchin, D. & Nunn, J., 2014. The invasive brown alga Undaria pinnatifida (Harvey) Suringar, 1873 (Laminariales: Alariaceae), spreads northwards in Europe. Bioinvasions Records, 3 (2), 57-63. DOI http://dx.doi.org/10.3391/bir.2014.3.2.01

    103. Moore, P.G., 1973a. The kelp fauna of north east Britain I. Function of the physical environment. Journal of Experimental Marine Biology and Ecology, 13, 97-125.

    104. Moore, P.G., 1973b. The kelp fauna of north east Britain. II. Multivariate classification: turbidity as an ecological factor. Journal of Experimental Marine Biology and Ecology, 13, 127-163.

    105. Moore, P.G., 1978. Turbidity and kelp holdfast Amphipoda. I. Wales and S.W. England. Journal of Experimental Marine Biology and Ecology, 32, 53-96.

    106. Moore, P.G., 1985. Levels of heterogeneity and the amphipod fauna of kelp holdfasts. In The Ecology of Rocky Coasts: essays presented to J.R. Lewis, D.Sc. (ed. P.G. Moore & R. Seed), 274-289. London: Hodder & Stoughton Ltd.

    107. Munda, I.M. & Luning, K., 1977. Growth performance of Alaria esculenta off Helgoland. Helgolander Wissenschaftliche Meeresuntersuchungen, 29, 311-314.

    108. NBN, 2015. National Biodiversity Network 2015(20/05/2015). https://data.nbn.org.uk/

    109. Nichols, D., 1981. The Cornish Sea-urchin Fishery. Cornish Studies, 9, 5-18.

    110. Norderhaug, K., 2004. Use of red algae as hosts by kelp-associated amphipods. Marine Biology, 144 (2), 225-230.

    111. Norderhaug, K.M. & Christie, H.C., 2009. Sea urchin grazing and kelp re-vegetation in the NE Atlantic. Marine Biology Research, 5 (6), 515-528.

    112. Norderhaug, K.M., Christie, H. & Fredriksen, S., 2007. Is habitat size an important factor for faunal abundances on kelp (Laminaria hyperborea)? Journal of Sea Research, 58 (2), 120-124.

    113. Nordheim, van, H., Andersen, O.N. & Thissen, J., 1996. Red lists of Biotopes, Flora and Fauna of the Trilateral Wadden Sea area, 1995. Helgolander Meeresuntersuchungen, 50 (Suppl.), 1-136.

    114. Norton, T.A., 1992. Dispersal by macroalgae. British Phycological Journal, 27, 293-301.

    115. Norton, T.A., Hiscock, K. & Kitching, J.A., 1977. The Ecology of Lough Ine XX. The Laminaria forest at Carrigathorna. Journal of Ecology, 65, 919-941.

    116. Pedersen, M.F., Nejrup, L.B., Fredriksen, S., Christie, H. & Norderhaug, K.M., 2012. Effects of wave exposure on population structure, demography, biomass and productivity of the kelp Laminaria hyperborea. Marine Ecology Progress Series, 451, 45-60.

    117. Penfold, R., Hughson, S., & Boyle, N., 1996. The potential for a sea urchin fishery in Shetland. http://www.nafc.ac.uk/publish/note5/note5.htm, 2000-04-14

    118. Pérez, R., 1971. Écologie, croissance et régénération, teneurs en acide alginique de Laminaria digitata sur les cotes de la Manche. Revue des Travaux de l'Institut des Peches Maritimes, 35, 287-346.

    119. Philippart, C.J., Anadón, R., Danovaro, R., Dippner, J.W., Drinkwater, K.F., Hawkins, S.J., Oguz, T., O'Sullivan, G. & Reid, P.C., 2011. Impacts of climate change on European marine ecosystems: observations, expectations and indicators. Journal of Experimental Marine Biology and Ecology, 400 (1), 52-69.

    120. Raffaelli, D.G.  & Hawkins, S.J., 1999. Intertidal Ecology 2nd edn.. London: Kluwer Academic Publishers.

    121. Rinde, E. & Sjøtun, K., 2005. Demographic variation in the kelp Laminaria hyperborea along a latitudinal gradient. Marine Biology, 146 (6), 1051-1062.

    122. Rostron, D.M. & Bunker, F. St P.D., 1997. An assessment of sublittoral epibenthic communities and species following the Sea Empress oil spill. A report to the Countryside Council for Wales from Marine Seen & Sub-Sea Survey., Countryside Council for Wales, Bangor, CCW Sea Empress Contact Science, no. 177.

    123. Schiel, D.R. & Foster, M.S., 1986. The structure of subtidal algal stands in temperate waters. Oceanography and Marine Biology: an Annual Review, 24, 265-307.

    124. Schiel, D.R. & Taylor, D.I., 1999. Effects of trampling on a rocky intertidal algal assemblage in southern New Zealand. Journal of Experimental Marine Biology and Ecology, 235, 213-235.

    125. Seapy , R.R. & Littler, M.M., 1982. Population and Species Diversity Fluctuations in a Rocky Intertidal Community Relative to Severe Aerial Exposure and Sediment Burial. Marine Biology, 71, 87-96.

    126. Sheppard, C.R.C., Bellamy, D.J. & Sheppard, A.L.S., 1980. Study of the fauna inhabiting the holdfasts of Laminaria hyperborea (Gunn.) Fosl. along some environmental and geographical gradients. Marine Environmental Research, 4, 25-51.

    127. Sivertsen, K., 1997. Geographic and environmental factors affecting the distribution of kelp beds and barren grounds and changes in biota associated with kelp reduction at sites along the Norwegian coast. Canadian Journal of Fisheries and Aquatic Sciences, 54, 2872-2887.

    128. Sjøtun, K., Christie, H. & Helge Fosså, J., 2006. The combined effect of canopy shading and sea urchin grazing on recruitment in kelp forest (Laminaria hyperborea). Marine Biology Research, 2 (1), 24-32.

    129. Sjøtun, K. & Schoschina, E.V., 2002. Gametophytic development of Laminaria spp. (Laminariales, Phaeophyta) at low temperatures. Phycologia, 41, 147-152.

    130. Smale, D.A., Burrows, M.T., Moore, P., O'Connor, N. & Hawkins, S.J., 2013. Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and evolution, 3 (11), 4016-4038.

    131. Smale, D.A., Wernberg, T., Yunnie, A.L. & Vance, T., 2014. The rise of Laminaria ochroleuca in the Western English Channel (UK) and comparisons with its competitor and assemblage dominant Laminaria hyperborea. Marine ecology.

    132. Smith, J.E. (ed.), 1968. 'Torrey Canyon'. Pollution and marine life. Cambridge: Cambridge University Press.

    133. Somerfield, P.J. & Warwick, R.M., 1999. Appraisal of environmental impact and recovery using Laminaria holdfast faunas. Sea Empress, Environmental Evaluation Committee., Countryside Council for Wales, Bangor, CCW Sea Empress Contract Science, Report no. 321.

    134. Staehr, P.A., Pedersen, M.F., Thomsen, M.S., Wernberg, T. & Krause-Jensen, D., 2000. Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Marine Ecology Progress Series, 207, 79-88. DOI https://doi.org/10.3354/meps207079

    135. Steneck, R.S., Graham, M.H., Bourque, B.J., Corbett, D., Erlandson, J.M., Estes, J.A. & Tegner, M.J., 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental conservation, 29 (04), 436-459.

    136. Steneck, R.S., Vavrinec, J. & Leland, A.V., 2004. Accelerating trophic-level dysfunction in kelp forest ecosystems of the western North Atlantic. Ecosystems, 7 (4), 323-332.

    137. Strong, J.A. & Dring, M.J., 2011. Macroalgal competition and invasive success: testing competition in mixed canopies of Sargassum muticum and Saccharina latissima. Botanica Marina, 54 (3), 223-229.

    138. Sundene, O., 1962. The implications of transplant and culture experiments on the growth and distribution of Alaria esculenta. Nytt Magasin for Botanik, 9, 155-174.

    139. Teagle, H., Hawkins, S. J., Moore, P. J. & Smale, D. A., 2017. The role of kelp species as biogenic habitat formers in coastal marine ecosystems. Journal of Experimental Marine Biology and Ecology, 492, 81-98. DOI https://doi.org/10.1016/j.jembe.2017.01.017

    140. Thompson, G.A. & Schiel, D.R., 2012. Resistance and facilitation by native algal communities in the invasion success of Undaria pinnatifida. Marine Ecology, Progress Series, 468, 95-105.

    141. Tidbury, H, 2020. Wakame (Undaria pinnatifida). GB Non-native Species Rapid Risk Assessment., 15 pp. Available from: http://www.nonnativespecies.org/index.cfm?pageid=143

    142. Vadas, R.L. & Elner, R.W., 1992. Plant-animal interactions in the north-west Atlantic. In Plant-animal interactions in the marine benthos, (ed. D.M. John, S.J. Hawkins & J.H. Price), 33-60. Oxford: Clarendon Press. [Systematics Association Special Volume, no. 46].

    143. Vadas, R.L., Johnson, S. & Norton, T.A., 1992. Recruitment and mortality of early post-settlement stages of benthic algae. British Phycological Journal, 27, 331-351.

    144. Van den Hoek, C., 1982. The distribution of benthic marine algae in relation to the temperature regulation of their life histories. Biological Journal of the Linnean Society, 18, 81-144.

    145. Vaz-Pinto, F., Rodil, I.F., Mineur, F., Olabarria, C. & Arenas, F., 2014. Understanding biological invasions by seaweeds. In Pereira, L. & Neto, J.M. (eds.). Marine algae: biodiversity, taxonomy, environmental assessment and biotechnology. Boca Raton, Florida: CRC Press, pp. 140-177.

    146. Viejo, R.M., Arrontes, J. & Andrew, N.L., 1995. An Experimental Evaluation of the Effect of Wave Action on the Distribution of Sargassum muticum in Northern Spain. , 38 (1-6), 437-442. DOI https://doi.org/10.1515/botm.1995.38.1-6.437

    147. Vost, L.M., 1983. The influence of Echinus esculentus grazing on subtidal algal communities. British Phycological Journal, 18, 211.

    148. Whittick, A., 1983. Spatial and temporal distributions of dominant epiphytes on the stipes of Laminaria hyperborea (Gunn.) Fosl. (Phaeophyta: Laminariales) in S.E. Scotland. Journal of Experimental Marine Biology and Ecology, 73, 1-10.

    149. Wotton, D.M., O'Brien, C., Stuart, M.D. & Fergus, D.J., 2004. Eradication success down under: heat treatment of a sunken trawler to kill the invasive seaweed Undaria pinnatifida. Marine Pollution Bulletin, 49 (9), 844-849.

    Citation

    This review can be cited as:

    Stamp, T.E., Tyler-Walters, H., & Burdett, E.G. 2023. Alaria esculenta on exposed sublittoral fringe bedrock. In Tyler-Walters H. and Hiscock K. (eds) Marine Life Information Network: Biology and Sensitivity Key Information Reviews, [on-line]. Plymouth: Marine Biological Association of the United Kingdom. [cited 08-10-2024]. Available from: https://www.marlin.ac.uk/habitat/detail/165

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