Laminaria hyperborea forest with a faunal cushion (sponges and polyclinids) and foliose red seaweeds on very exposed upper infralittoral rock

Summary

UK and Ireland classification

Description

Very exposed and exposed, but wave-surged, upper infralittoral bedrock and massive boulders characterised by a dense forest of the kelp Laminaria hyperborea with a high diversity of seaweeds and invertebrates. The shallowest kelp plants are often short or stunted, while deeper plants are taller with heavily epiphytised stipes with foliose red seaweeds such as Delesseria sanguinea, Cryptopleura ramosa or Plocamium cartilagineum or even the brown seaweed Dictyota dichotoma. Also found on the stipes or on the rock below the canopy are red seaweeds including Phycodrys rubens, Kallymenia reniformis, Metacallophyllis laciniata, Caryophyllia smithii, and Corallina officinalis, while encrusting coralline algae can cover any bare patches of rock. At some sites the red seaweeds can be virtually mono-specific, while at other sites show considerable variation containing a dense mixed turf of a large variety of species. The red seaweed Odonthalia dentata can be present in the north. The faunal and floral under-storey is generally rich in species due, in part, to the relatively low urchin-grazing pressure in such shallow exposed conditions. The faunal composition of this biotope varies markedly between sites, but commonly occurring are the soft coral Alcyonium digitatum and the anthozoans Cylista elegans and Corynactis viridis. Sponges form a prominent part of the community with variable amounts of the sponges Halichondria panicea and Pachymatisma johnstonia and several other species. The crab Cancer pagurus and the starfish Asterias rubens are normally present in small numbers foraging beneath the canopy, while the sea urchins Echinus esculentus and Urticina felina graze on the seaweeds. The hydroid Obelia geniculata, the ascidian Botryllus schlosseri and the bryozoan Membranipora membranacea compete for space on the kelp, whereas the bryozoan Electra pilosa also can be found on foliose red seaweeds.

This kelp forest most commonly occurs beneath a zone of Alaria esculenta and Mytilus edulis (Ala.Myt) and may contain small patches of Alaria esculenta. As the force of the wave-surge diminishes with increased depth, density of the faunal turf reduces and the kelp forest or park changes to one characterized by kelp and dense red seaweeds (LhypR.Ft or LhypR.Pk). In some areas of Shetland and St Kilda the lower infralittoral zone is characterised by a park of the kelp Saccharina latissima and/or Saccorhiza polyschides (SlatSac). Where the Laminaria hyperborea forest continues to depths of 15 m or greater it may give way to a zone of dense foliose red algae (FoR or For.Dic). (Information from Connor et al., 2004; JNCC, 2015, 2022).

Depth range

0-5 m, 5-10 m, 10-20 m

Additional information

-

Listed By

Habitat review

Ecology

Ecological and functional relationships

This is an extremely dynamic biotope with the main rock cover species that occupy it competing for space and significant seasonal changes occurring. In shallow depths, suspension feeding animal species may out-compete algae and dominate even in well-lit areas. Also, sea urchins are often absent from shallow (say, less than 10m) depths due to strong wave action thus allowing a much more lush growth of algae than would be the case if grazing was occurring. Kelps are major primary producers and up to 90 percent of kelp production enters the detrital food web so that kelp is probably a major contributor of organic carbon to surrounding communities (Birkett et al. 1998b). Kelp fronds, stipes and holdfasts provide substrata for distinct communities of species, some of which are found only or especially on kelp plants. Hiscock & Mitchell (1980) list 15 species of algae associated with kelp stipes in the UK. The stipes also support epifaunal bryozoa and hydroids (Norton et al. 1977). Holdfasts support a diverse fauna that represents a sample of the surrounding mobile fauna and crevice dwelling organisms, e.g., polychaetes, small crabs, gastropods, bivalves, and amphipods. Jones (1971) lists 53 macrofaunal invertebrates in holdfasts and Moore (1973) reports 389 species from holdfasts collected in the north east coast of Britain. An account of holdfast fauna is given by Hayward (1988). Where sea-urchins occur, they graze the undercanopy and understorey algae, including juvenile kelp sporophytes, together with epiphytes and epifauna on the lower reaches of the laminarian stipe. Sea urchin grazing may maintain the patchy and species rich understorey epiflora/fauna by preventing a small number of species from becoming dominant. Vost (1983) examined the effect of removing grazing Echinus esculentus and found that after 6-10 months the patchiness of the understorey algae had decreased and the species richness and biomass of epilithic species increased. Echinus esculentus grazing probably controls the lower limit of Laminaria hyperborea distribution in some location, e.g. in the Isle of Man (Jones & Kain 1967; Kain et al. 1974; Kain 1979). Other ecological relationships are:

  • Epiphytes and understorey algae are grazed by a variety of amphipods, isopods and gastropods, e.g. Littorina spp., Acmaea spp., Aplysia and rissoid gastropods (Birkett et al. 1988b).
  • Lobsters (Homarus gammarus), crabs and some fish species (e.g. the wolffish Anarchicas lupus) and perhaps otters are known to consume gastropod and echinoderm grazers.
  • Kelp communities and the interaction between kelp, urchins and predators has been studied in Nova Scotia, Norway, southern California and the UK (Mann 1982; Kain 1979; Sivertsen 1997; Vadas & Elner 1992; Elner & Vadas, 1990; Schiel & Foster, 1986).
  • Birkett et al. (1998b) suggest that juveniles of animals present in kelp beds as adults probably use the habitat as a nursery and unknown numbers of species are likely to use the habitat during their life cycle. Rinde et al. (1992 cited in Birkett et al. 1998b) state that Norwegian kelp beds are nurseries for gadoid species.
  • The composition of the holdfast fauna has been show to vary with turbidity (natural and anthropogenic in origin), between kelp species (due to holdfast architecture and volume), and with location around the coast of the British Isles (Moore 1973a&b; Moore 1978; Edwards 1980; Sheppard et al. 1980). Moore (1973a&b) identified groups of species that were found in most cases, or restricted to either turbid or clear waters. Moore (1978) noted that species diversity or amphipods decreased with increasing turbidity, partly due to the increased dominance of a few species. Edwards (1980) noted that holdfast fauna in south-west Ireland were numerically dominated by suspension feeders with decreasing numbers of omnivores and carnivores respectively. Edwards (1980) noted that holdfasts were dominated by Spirobranchus triqueter in the most turbid sites, although these were not as turbid as sites examined by Moore (1973a&b). Along the North Sea coast species number and diversity increased with increased clarity, however where heavy metals were a factor species number and diversity decreased with increasing heavy metal pollution. They were able to distinguish groups of species characteristic of all sites, or clear or turbid sties. Along the west coast both heavy metals and turbidity were important. Where turbidity and heavy metals increased suspension feeders increased in abundance while other trophic groups decreased. However, along the south coast longitude was the most important factor, and they suggested that natural variation in temperature, salinity and water flow were responsible for variation between holdfast communities (Sheppard et al. 1980). Moore (1985) also demonstrated that the amphipod fauna varied with water flow rate (resulting from wave action and currents); for example sites of increased exposure were dominated by Amphithoe rubricata, Lembos websteri and Jassa falcata whereas Gitana sarsi, Dexamine thea and Corophium bonnellii flourish in wave sheltered environments.
  • A few meiofaunal species may burrow into kelp tissue, e.g. the nematode Monohystera disjuncta (Birkett et al. 1998b).
  • The understorey flora varies with location, depth, exposure, hydrographic regime, turbidity and siltation and may be sparse or species rich. Birkett et al. (1998b; Appendix 5) list 52 common kelp biotope understorey algae in the UK including characterizing species such us Delesseria sanguinea, Dictyota dichotoma, Phycodrys rubens, Cryptopleura ramosa, Plocamium cartilagineum, and Metacallophyllis laciniata.
  • The benthic fauna varies with depth, exposure, location and substratum, however, no species are specific to kelp forest. Norton et al. (1977) demonstrate the zonation of 22 epibenthic species. However, many species, both fixed and mobile, are present and probably under recorded (Birkett et al. 1998b).

Seasonal and longer term change

The species present in the biotope are believed to be mainly present throughout the year. However, many algae will show a seasonal change from recruitment of ephemeral species and re-growth of perennial species in the spring, through growth of epibiota on the algae in summer and degeneration of fronds in many species in the autumn and winter. New blades of Laminaria hyperborea grow in winter between the meristem and the old blade, which is shed in early spring or summer together with associated species growing on its surface. Larger and older kelp plants become liable to removal by wave action and storms due to their size and weakening by grazers such as Patella pellucida. There is therefore likely to be a reduced abundance of kelps following the winter. Loss of older plants results in more light reaching the understorey, temporarily permitting growth of algae including Laminaria hyperborea sporelings. Areas of kelp may become denuded of macroalgae at intervals and the substrata dominated by encrusting corallines. These areas are often associated with an increase in urchin numbers forming 'fronts' of small and large urchins that remove large quantities of algae including the kelps themselves forming 'urchin barrens'. Sea urchin grazing is an important factor in kelp beds and, as part of the biotope, the following suggested factors affecting sea urchin populations are presented.

  • Several predators have been suggested as controlling sea urchin populations e.g. sea otters, lobsters, crabs or wolffish, however the evidence is equivocal (Birkett et al 1998b; Elner & Vadas 1990; Mann 1982).
  • Evidence suggests that sea urchin recruitment is sporadic and may be enhanced by low temperatures (Birkett et al. 1998b).
  • Sea urchin recruitment is also enhanced by the presence of 'urchin barrens' presumably due to the lack of suspension feeders that would otherwise consume their larvae (Lang & Mann 1978).
  • Sea urchin diseases, such as 'bald-urchin' disease, encouraged by high water temperatures drastically reduce the urchin population (Lobban & Harrison, 1997). However, although parasitic infections are found in Echinus esculentus, no evidence of sea urchin disease has been found in the UK.
  • Sivertsen (1997) examined grazing of west and north Norwegian coast Laminaria hyperborea beds by Strongylocentrotus droebachiensis and Echinus esculentus. He concluded that seven environmental factors contributed to the distribution of kelp beds and 'barrens': depth gradient, latitude, time of sampling, nematode infection (in Strongylocentrotus droebachiensis), wave exposure, coastal gradient and substratum.

The factors controlling sea urchin populations and 'urchin barrens' in kelp beds is poorly understood, especially in the UK, However, it is likely that the local urchin population is controlled by a number of factors that vary between sites and biotopes; including predators, competition for food with other grazers, variation in sea urchin recruitment, and parasitic infection or disease.
Periodic storms are likely to remove older and weaker plants creating patches cleared of kelp and increasing the local turbidity. While cleared patches may encourage growth of sporelings or gametophyte maturation, they may also enhance sea urchin recruitment.

Habitat structure and complexity

Kelp beds are diverse species rich habitats and over 1,800 species have been recorded in the UK kelp biotopes (Birkett et al. 1998b). Kelp forest provides a variety of habitats and refugia in a similar way to terrestrial forests. Kelps also reduce current flow producing a sheltered microclimate. In kelp forests (e.g. EIR.LhypR.Ft) the kelp density produces a canopy which excludes up to 90% of incident light allowing many deeper water, shade tolerant algae, mainly reds, to invade. In deeper water, as light intensity decreases, the kelp density decreases forming a kelp park (Norton et al. 1977). Kelp beds are patchy and dynamic with areas devoid of kelp (due to storms, wave surge or grazing) in the process of expansion or recolonization in different stages of succession. Species diversity changes with depth, between forest & park, with exposure, substratum and turbidity (Birkett et al. 1998b; Erwin et al. 1990; Norton et al. 1977).  Wrasse and pollock have been observed associated especially with kelp forests and epibenthic predatory or herbivorous fish are also found, e.g. blennies, gobies and wolffish (Anarhichas lupus).

Productivity

Kelps are the major primary producers in UK marine coastal waters producing nearly 75 percent of the net carbon fixed annually on the shoreline of the coastal euphotic zone (Birkett et al. 1998b). Kelp plants produce 2.7 times their standing biomass per year. Kelp detritus, as broken plant tissue, particles and dissolved organic material supports soft bottom communities outside the kelp bed itself. The kelps reduce ambient levels of nutrients, although this may not be significant in exposed sites, but increase levels of particulate and dissolved organic matter within the bed.

Recruitment processes

Recruitment processes of key characteristic or dominant species are described here. Laminaria hyperborea produces vast numbers of spores, however they need to settle and form gametophytes within about 1 mm of each to ensure fertilisation and therefore may suffer from dilution effects over distance. Gametophytes can survive darkness and develop in the low light levels under the canopy. However, young sporelings develop slowly in low light. Loss of older plants provides the opportunity to develop into adult plants. Recruitment in Echinus esculentus is sporadic or annual depending on location and may benefit from the presence of 'urchin barrens'. Patella pellucida is an annual species, larvae settling in the lower eulittoral and juveniles migrating to kelp ,via several algal species, as they grow. (Please view individual key information reviews for details). Epifaunal larvae probably contribute to the plankton of the kelp bed and many are lost to the suspension feeding epifauna. Kelp beds also provide nurseries for larvae and fish species (see above). Recruitment of epiphytes and epiflora are dependant on dispersal and settlement of algal spores and survival of early post-settlement stages. Norton (1992) suggests that spore dispersal in primarily dependant on currents and eddies. Settlement of algal spores is partly dependant on their motility (if any) and adhesive properties together with preferences for topography (surface roughness), the chemical nature of the substratum and water movement (Norton 1992; Fletcher & Callow 1992). Vadas et al. 1992 suggested that survival of early post settlement stages is dependant on grazing, the algal canopy and turf effects together with desiccation and water motion, and they further suggest that recruitment is likely to be episodic, variable and to suffer from high mortality of early stages. Kain (1975) examined recolonization of artificially cleared areas in a Laminaria hyperborea forest in Port Erin, Isle of Man. Cleared concrete blocks were colonized by Saccorhiza polychides, Alaria esculenta, Desmarestia spp., Laminaria hyperborea, Laminaria digitata, Saccharina latissima (studied as Laminaria saccharina) and un-specified Rhodophyceae at 0.8m. Saccorhiza polychides dominated within 8 months but had virtually disappeared with 77 weeks to be replaced by laminarians, including Alaria esculenta. After about 2.5 years, Laminaria hyperborea standing crop, together with an understorey of red algae (Rhodophyceae), was similar to that of virgin forest. Rhodophyceae were present throughout the succession increasing from 0.04 to 1.5 percent of the biomass within the first 4 years. Colonizing species varied with time of year, for example blocks cleared in August 1969 were colonized by primarily Saccharina latissima and subsequent colonization by Laminaria hyperborea and other laminarians was faster than blocks colonized by Saccorhiza polychides; within 1 year the block was occupied by laminarians and Rhodophyceae only. Succession was similar at 4.4m, and Laminaria hyperborea dominated within about 3 years. Blocks cleared in August 1969 at 4.4m were not colonized by Saccorhiza polychides but were dominated by Rhodophyceae after 41 weeks, e.g. Delesseria sanguineaand Cryptopleura ramosa. Kain (1975) cleared one group of blocks at two monthly intervals and noted that Phaeophyceae were dominant colonists in spring, Chlorophyceae (solely Ulva lactuca) in summer and Rhodophyceae were most important in autumn and winter. Animal species are likely to recruit mainly from the plankton although some species such as polyclinid tunicates may have larva that swim for only 2-3 hours (Berril 1950) or no larval stage (amphipods). Little is known about the reproductive biology and dispersal of some species but information from clearance experiments (see 'Time for community to reach maturity') suggests that sponges may be slow to settle.

Time for community to reach maturity

Experimental clearance experiments in the Isle of Man (Kain 1975; Kain, 1979) showed that Laminaria hyperborea out-competed other opportunistic species (e.g. Alaria esculenta, Saccorhiza polyschides and Desmarestia spp.) and returned to near control levels of biomass within 3 years at 0.8 m but that recovery was slower at 4.4m (see above). Kain (1979) noted that grazing would slow recovery as few sporophytes survived after 1 year in the presence of Echinus esculentus. However, the presence of other kelps and Desmarestia spp. (the latter is distasteful to grazers due to presence of sulphuric acids in its tissue) may act as refugia from grazing for developing Laminaria hyperborea juveniles that eventually out-compete the other species. Studies of the effects of harvesting in Norway (Svendsen 1972 cited in Birkett et al. 1998b) showed that kelp biomass returned 3-4 years after harvesting, although the plants were small (about 1m) and the age class was shifted towards younger plants. Sivertsen (1991 cited in Birkett et al. 1998b), showed that kelp populations stabilise about 4-5 years after harvesting. Re-growth partly due to growth of viable juveniles remaining after harvesting. Current advice suggests that kelp forest should be left 7-10 years for kelp and non-kelp species to recover (Birkett et al. 1998b). Detailed studies in Norway by Rinde et al. (1992 cited in Birkett et al. 1998b) examined recovery of non-kelp species. The epiphyte community in control areas about 10 years old was richer and more extensive than on replacement plants in harvested areas. Of the epifauna, Halichondria sp. were only found on 10 year old plants and tunicates on plants 6 years post harvesting. Holdfast fauna was more abundant richer in 10 year old plants in control areas than younger plants in previously harvested area. Older plants have larger holdfasts. Shrimp, lobster, hermit crabs, Echinus esculentus and Strongylocentrotus droebachiensis were associated with holdfasts in control areas but absent from harvested areas. Control areas had a more diverse benthic macroflora and macrofauna. Dredged areas exhibited growth of opportunistic kelps e.g. Alaria esculenta and also Desmarestia spp. while the bottom was covered by coralline algae between young Laminaria hyperborea after 3 years. Control areas had a more diverse bottom community. Overall his results suggest that full biological recovery, or maturation, may take at least 10 years.

Additional information

-

Preferences & Distribution

Habitat preferences

Depth Range 0-5 m, 5-10 m, 10-20 m
Water clarity preferences
Limiting Nutrients No information
Salinity preferences Full (30-40 psu)
Physiographic preferences Open coast
Biological zone preferences Upper infralittoral
Substratum/habitat preferences Bedrock, Large to very large boulders
Tidal strength preferences Moderately strong 1 to 3 knots (0.5-1.5 m/sec.), Strong 3 to 6 knots (1.5-3 m/sec.), Weak < 1 knot (<0.5 m/sec.)
Wave exposure preferences Exposed, Extremely exposed, Very exposed
Other preferences High wave exposure

Additional Information

Species composition

Species found especially in this biotope

    Rare or scarce species associated with this biotope

    -

    Additional information

    The biotope is defined by conspicuous species but is probably rich in a wide range of other mobile animal species especially amongst the foliose algae, in kelp holdfasts and attached to the kelp stipes and fronds.

    Sensitivity review

    Sensitivity characteristics of the habitat and relevant characteristic species

    At high densities, Laminaria hyperborea forms a canopy over infralittoral rock. Beneath the canopy an understorey community grows, typically defined by a red seaweed turf although faunal species dominate in tide-swept and/or wave surged conditions. Grazing by the urchins; Echinus esculentus and Paracentrotus lividus can also define the biotope and reduce the biomass of Laminaria hyperborea and understorey flora. The abundance of Laminaria hyperborea is determined by light availability, which decreases with an increase in water depth. Therefore, depth and water clarity determine the density of Laminaria and hence the distribution of kelp forest (high density kelp) and park (low density kelp) sub-biotopes.

    Kelp biotopes are a major source of primary productivity and support magnified secondary productivity within North Atlantic coastal waters (Smale et al., 2013, Brodie et al., 2014). In Scotland alone, kelp biotopes are estimated to cover 8000 km2 (Walker, 1953), and account for ca 45% of primary production in UK coastal waters (Smale et al., 2013). Therefore, kelp biotopes, of which Laminaria hyperborea is dominant within UK subtidal rocky reefs (Birkett et al., 1998b), make a substantial contribution to coastal primary production in the UK (Smale et al., 2013). Laminaria hyperborea is grazed directly by species such as Patella pellucida, however, approximately 80% of primary production is consumed as detritus or dissolved organic material (Krumhansl, 2012), which is both retained within and transported out of the parent kelp forest, providing valuable nutrition to potentially low productivity habitats such as sandy beaches (Smale et al., 2013).

    Laminaria hyperborea also acts as an ecosystem engineer (Jones et al., 1996; Smale et al., 2013) by altering; light levels (Sjøtun et al., 2006), physical disturbance (Connell, 2003), sedimentation rates (Eckman et al., 1989) and water flow (Smale et al., 2013), profoundly altering the physical environment for fauna and flora in close proximity. Laminaria hyperborea biotopes increase the three-dimensional complexity of unvegetated rock (Norderhaug, 2004, Norderhaug et al., 2007, Norderhaug & Christie, 2011, Gorman et al., 2012; Smale et al., 2013) and support high local diversity, abundance and biomass of epi/benthic species (Smale et al., 2013), and serve as a nursery ground for a number of commercially important species, e.g. Gadidae (The taxonomic family that contains many commercially important marine fish species, including the Atlantic Cod and Pollack) (Rinde et al., 1992).

    In undertaking this assessment of sensitivity, an account is taken of knowledge of the biology of all characterizing species/taxa in the biotope. For this sensitivity assessment, Laminaria hyperborea is the primary focus of research, however, it is recognized that the understorey community, typically red seaweeds, also define the biotope. Examples of important species groups are mentioned where appropriate.

    Resilience and recovery rates of habitat

    A number of review and experimental publications have assessed the recovery of Laminaria hyperborea kelp beds and the associated community. If environmental conditions are favourable Laminaria hyperborea can recover following disturbance events reaching comparable plant densities and size to pristine Laminaria hyperborea beds within 2-6 years (Kain, 1979; Birkett et al., 1998b; Christie et al., 1998). Holdfast communities may recover in 6 years (Birkett et al., 1998b). Full epiphytic community and stipe habitat complexity regeneration require over 6 years (possibly 10 years). These recovery rates were based on discrete kelp harvesting events.  Recurrent disturbance occurring frequently within 2-6 years of the initial disturbance is likely to lengthen recovery time (Birkett et al., 1998b, Burrows et al., 2014). Kain (1975) cleared sublittoral blocks of Laminaria hyperborea at different times of the year for several years. The first colonizers and succession community differed between blocks and at what time of year the blocks were cleared, however within 2 years of clearance the blocks were dominated by Laminaria hyperborea (Fletcher et al., 2006).

    In south Norway, Laminaria hyperborea forests are harvested, which results in large scale removal of the canopy-forming kelps.  Cristie et al., (1998) found that in south Norwegian Laminaria hyperborea beds a pool of small (<25cm) understorey Laminaria hyperborea plants persist beneath the kelp canopy for several years. The understorey Laminaria hyperborea sporophytes had fully re-established the canopy at a height of 1m within 2-6 years after kelp harvesting. Within 1 year following harvesting, and each successive year thereafter, a pool of Laminaria hyperborea recruits had re-established within the understorey beneath the kelp canopy. Cristie et al., (1998) suggested that Laminaria hyperborea bed re-establishment from understorey recruits (see above) inhibits the colonization of other kelps species and furthers the dominance of Laminaria hyperborea within suitable habitats, stating that Laminaria hyperborea habitats are relatively resilient to disturbance events.

    Laminaria hyperborea has a heteromorphic life strategy, A vast number of zoospores (mobile asexual spores) are released into the water column between October-April (Kain & Jones, 1964). Zoospores settle onto rock substrata and develop into dioecious gametophytes (Kain, 1979) which, following fertilization, develop into sporophytes and mature within 1-6 years (Kain, 1979; Fredriksen et al., 1995; Christie et al., 1998).  Laminaria hyperborea zoospores have a recorded dispersal range of ~200m (Fredriksen et al., 1995). However zoospore dispersal is greatly influenced by water movements, and zoospore density and the rate of successful fertilization decreases exponentially with distance from the parental source (Fredriksen et al., 1995). Hence, recruitment following disturbance can be influenced by the proximity of mature kelp beds producing viable zoospores to the disturbed area. (Kain, 1979, Fredriksen et al., 1995).

    Laminaria hyperborea biotopes are partially reliant on low (or no) populations of sea urchins, primarily the species; Echinus esculentus, Paracentrotus lividus and Strongylocentrotus droebachiensis, which graze directly on macroalgae, epiphytes and the understorey community.  Multiple authors (Steneck et al., 2002; Steneck et al., 2004; Rinde & Sjøtun, 2005; Norderhaug & Christie, 2009; Smale et al., 2013) have reported dense aggregations of sea urchins to be a principal threat to Laminaria hyperborea biotopes of the North Atlantic. Intense urchin grazing creates expansive areas known as “urchin barrens”, in which a shift can occur from Laminaria hyperborea dominated biotopes to those characterized by coralline encrusting algae, with a resultant reduction in biodiversity (Leinaas & Christie, 1996; Steneck et al., 2002; Norderhaug & Christie, 2009). Continued intensive urchin grazing pressure on Laminaria hyperborea biotopes can inhibit the Laminaria hyperborea recruitment (Sjøtun et al., 2006) and cause urchin barrens to persist for decades (Cristie et al., 1998; Stenneck et al., 2004; Rinde & Sjøtun, 2005). The mechanisms that control sea urchin aggregations are poorly understood but have been attributed to anthropogenic pressure on top down urchin predators (e.g. cod or lobsters). While these theories are largely unproven, a number of studies have shown that removal of urchins from grazed areas coincides with kelp re-colonization (Leinaas & Christie, 1996; Norderhaug & Christie, 2009). Leinaas & Christie, (1996) removed Strongylocentrotus droebachiensis from “urchin barrens” and observed a succession effect, in which the substratum was initially colonized by filamentous macroalgae and Saccharina latissima.  However, after 2-4 years, Laminaria hyperborea dominated the community.

    Reports of large-scale urchin barrens within the North East Atlantic are generally limited to regions of the North Norwegian and Russian Coast (Rinde & Sjøtun, 2005, Norderhaug & Christie, 2009). Within the UK, urchin grazed biotopes (IR.MIR.KR.Lhyp.GzFt/Pk, IR.HIR.KFaR.LhypPar, IR.LIR.K.LhypSlat.Gz & IR.LIR.K.Slat.Gz) are generally localised to a few regions in North Scotland and Ireland (Smale et al., 2013; Stenneck et al., 2002; Norderhaug & Christie 2009; Connor et al., 2004). IR.MIR.KR.Lhyp.GzFt/Pk, IR.HIR.KFaR.LhypPar, IR.LIR.K.LhypSlat.Gz & IR.LIR.K.Slat.Gz are characterized by canopy-forming kelp. However, urchin grazing decreases the abundance and diversity of understorey species. In the Isle of Man, Jones & Kain (1967) observed low Echinus esculentus grazing pressure can control the lower limit of Laminaria hyperborea and remove Laminaria hyperborea sporelings and juveniles. Urchin abundances in “urchin barrens” have been reported as high as 100 individuals/m2 (Lang & Mann, 1978). Kain (1967) reported urchin abundances of 1-4/m2 within experimental plots of the Isle of Man. Therefore, while “urchin barrens” are not presently an issue within the UK, relatively low urchin grazing has been found to control the depth distribution of Laminaria hyperborea, negatively impact Laminaria hyperborea recruitment and reduce the understorey community abundance and diversity.

    Other factors that are likely to influence the recovery of Laminaria hyperborea biotopes is competitive interactions with Invasive Non-Indigenous Species  (INIS), e.g. Undaria pinnatifida (Smale et al., 2013; Brodie et al., 2014; Heiser et al., 2014), and/or the Lusitanian kelp Laminaria ochroleuca (Brodie et al., 2014; Smale et al., 2015). A predicted sea temperature rise in the North and Celtic seas of between 1.5-5°C over the next century (Philippart et al., 2011) is likely to create northward range shifts in many macroalgal species, including Laminaria hyperborea. Laminaria hyperborea is a northern (Boreal) kelp species, thus increases in seawater temperature is likely to affect the resilience and recoverability of Laminaria hyperborea biotopes with southerly distributions in the UK (Smale et al., 2013; Stenneck et al., 2002). Evidence suggests that the Lusitanian kelp Laminaria ochroleuca (Smale et al., 2015), and the INIS Undaria pinnatifida (Heiser et al., 2014) are competing with Laminaria hyperborea along the UK south coast and may displace Laminaria hyperborea from some subtidal rocky reef habitats. The wider ecological consequences of Laminaria hyperborea’ competition with Laminaria ochroleuca and Undaria pinnatifida are however as of yet unknown.

    Resilience assessment. The evidence suggests that beds of mature Laminaria hyperborea can regenerate from disturbance within a period of 1-6 years, and the associated community within 7-10 years. However, other factors such as competitive interactions with Laminaria ochroleuca and Undaria pinnatifida may limit recovery of Laminaria hyperborea biotopes following disturbance. Also, urchin grazing pressure is shown to limit Laminaria hyperborea recruitment and reduce the diversity and abundance of the understorey community and may limit habitat recovery following disturbance. Similarly, changes in kelp canopy structure may alter subcanopy environment conditions and therefore the understory algal assemblages could be influenced (Smale et al., 2020). The recovery of Laminaria hyperborea biotopes to disturbance from commercial harvesting in south Norway suggests that Laminaria hyperborea beds and the associated community could recover from a significant loss of canopy cover within 10 years. Hence, resilience has therefore been assessed as Medium. An exception is for permanent or ongoing (long-term) pressures where recovery is not possible as the pressure is irreversible in which case resilience is assessed as ‘Very low’ by default.

    Please note as in Northern Norway urchin grazing pressure could extend recovery/resilience of the Laminaria hyperborea biotopes >25 years. If intensive urchin grazing (as seen in Northern Norway) occurs in the UK resilience would be re-assessed as Very Low. However, because of the limited/ localised incidence of urchin grazing within the UK, urchin grazing on large scales (as in Northern Norway) has not been included in this general resilience assessment. The introduction of Invasive Non-Indigenous Species (INIS) will also inhibit the recovery of Laminaria hyperborea biotopes for an indeterminate amount of time, in these cases, resilience would need to be re-assessed as 'Very low'. Another factor that is beyond the scope of this sensitivity assessment is the presence of multiple concurrent synergistic or cumulative effects, which Smale et al. (2013) suggested could be more damaging than individual pressures.

    Climate Change Pressures

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

    ResistanceResilienceSensitivity
    Global warming (extreme) [Show more]

    Global warming (extreme)

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

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

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

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

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

    Evidence

    The distribution of kelp is strongly influenced by climatic conditions; therefore, kelp species are extremely sensitive to the ongoing ocean warming (Kain, 1979; Van Den Hoek, 1982; Breeman, 1990; Lüning, 1990; Assis et al., 2016; Smale, 2020). Northern distribution boundaries are set by winter temperatures that are lethal, or summer temperatures too low for growth and/or reproduction, whilst southern limits are set by high lethal summer temperatures or winter temperatures too high for induction of a crucial step in the life cycle (Breeman, 1990). Kelps have a high dependence on ocean temperatures, which make them highly vulnerable to ocean warming (Assis et al., 2014). Laminaria hyperborea is a cold- temperate kelp species, distributed from the Barents Sea down to the coast of Portugal (Schoschina, 1997). 

    Laminaria hyperborea has an optimum temperature for growth of 15°C, and an upper temperature limit of 21°C (Bolton & Lüning, 1982). At 17°C gamete survival is reduced (Steinhoff et al., 2008) and gametogenesis is inhibited at 21°C (Dieck, 1992). It is therefore likely that Laminaria hyperborea recruitment will be impaired at a sustained temperature increase of above 17°C. However, sporophytes can tolerate slightly higher temperatures of 20°C. Temperature tolerances for Laminaria hyperborea are also seasonally variable and temperature changes are less tolerated in winter months than summer months (Birkett et al., 1998b).

    There is evidence that climate change is already having an impact on Laminaria hyperborea populations in the English Channel. Poleward range expansion of the warm temperate Laminaria ochroleuca as a result of ocean warming has led to competition with Laminaria hyperborea in UK waters (Smale et al., 2015). Laminaria ochroleucawas not found in the UK last century.  But Laminaria ochroleuca has now increased its range to include the southwest of England (Smale et al., 2015) and the west coast of Ireland (Schoenrock et al., 2019). While, since 1970 Laminaria hyperborea has undergone a range constriction of ~250 km at its warm leading-edge (Frontier et al., 2021). 

    During the 2013-2014 Northeast Atlantic storm season, the UK was subjected to some of the most intense storms recorded within the past five years. A study by Smale & Vance. (2015) investigated the impacts of the storms on kelp canopies along the south coast of the UK, findings indicated monospecific canopies of Laminaria hyperborea were unaffected by the storms. However, the storms significantly altered a mixed canopy study site, composed of Laminaria ochroleuca, Saccharina latissima and Laminaria hyperborea. Therefore, if climate change continues to change species composition within kelp forests resistance to storm disturbance could be altered.

    Smale et al. (2015) found that Laminaria hyperborea suffered from much higher epiphytic loadings and lower productivity than its competitor Laminaria ochroleuca during the summer months, which reduced its competitive ability. The decreased competitive ability because of ocean warming corresponds to findings by Pessarrodona et al. (2018), who found a decrease in the size of Laminaria hyperborea plants along a north-south gradient in Scotland, with average maximum stipe lengths of over 150 cm, whereas in southern England they were less than 100 cm. Similarly, Smale et al. (2020b) observed clear differences between net primary productivity (NNP) and carbon standing stock of Laminaria hyperborea between the colder northern and warmer southern test sites in the UK, with NNP and standing stock being 1.5 and 2.5 times greater in the northern sites. Identifying ocean temperatures as a lively driver of productivity, with reduced NNP and standing stock observed in warmer waters (Smale et al., 2020b). 

    The decrease in productivity in southern England suggests that Laminaria hyperborea is already growing at suboptimal temperatures. Assis et al. (2018) predicted that under the highest emission scenario (RCP 8.5) the biogeographic range of Laminaria hyperborea will move northwards, and this retreat would lead to this species being lost from approximately 30% of the UK coastline.

    Subtidal red algae are less tolerant of temperature extremes than intertidal red algae, surviving between -2°C and 18-23°C (Lüning 1990; Kain & Norton, 1990). Temperature increases may affect growth, recruitment, or interfere with reproduction processes. For example, there is some evidence to suggest that blade growth in Delesseria sanguinea is delayed until ambient sea temperatures fall below 13°C.  Blade growth is also likely to be intrinsically linked to gametangia development (Kain, 1987), and maintenance of sea temperatures above 13°C may affect recruitment success.

    Sensitivity assessment. Laminaria hyperborea is already growing at suboptimal temperatures in the southern UK, based on evidence of its decreased productivity comparative to Scotland (Pessarrodona et al., 2018; Smale et al., 2020b), and predictions have estimated Laminaria hyperborea to be lost from the UK by 2100 as a result of warming (Brodie et al., 2014). Sea surface temperatures around the UK currently ranging from 6-19°C (Huthnance, 2010).  Under the middle emission scenario, a rise of 3°C could lead to maximum summer high temperatures in the south of the UK of 22°C. This is above the upper thermal limit of 21°C for Laminaria hyperborea (Bolton & Lüning, 1982), and is likely to lead to loss of this species from the south of England. Furthermore, biomass and plant size are expected to decrease as waters warm, with Scottish Laminaria hyperborea stipe lengths decreasing to lengths observed in southern England, leading to a decline in carbon assimilation, productivity and habitat quality. Therefore, resistance is assessed as ‘Medium’, and resilience is assessed as ‘Very Low’, as the loss is likely to be a long-term decline, due to the long-term nature of ocean warming. Therefore, this biotope is assessed as ‘Medium’ sensitivity to ocean warming under this scenario.

    For the high emission scenario and extreme scenario, this northward retreat of the distribution of Laminaria hyperborea is expected to increase. Under the high emission scenario it is expected to be lost from 30% of the coastline around the UK (Assis et al., 2018), and under the extreme scenario more is projected to be lost. Populations that remain around the UK will become less productive. Therefore, under these scenarios, resistance is assessed as ‘Low’, and resilience is assessed as ‘Very Low’. Therefore, this biotope IR.HIR.KFaR.LhypFa is assessed as ‘High’ sensitivity to ocean warming under this scenario.

    Low
    High
    High
    High
    Help
    Very Low
    High
    High
    High
    Help
    High
    High
    High
    High
    Help
    Global warming (high) [Show more]

    Global warming (high)

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

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

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

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

    Evidence

    The distribution of kelp is strongly influenced by climatic conditions; therefore, kelp species are extremely sensitive to the ongoing ocean warming (Kain, 1979; Van Den Hoek, 1982; Breeman, 1990; Lüning, 1990; Assis et al., 2016; Smale, 2020). Northern distribution boundaries are set by winter temperatures that are lethal, or summer temperatures too low for growth and/or reproduction, whilst southern limits are set by high lethal summer temperatures or winter temperatures too high for induction of a crucial step in the life cycle (Breeman, 1990). Kelps have a high dependence on ocean temperatures, which make them highly vulnerable to ocean warming (Assis et al., 2014). Laminaria hyperborea is a cold- temperate kelp species, distributed from the Barents Sea down to the coast of Portugal (Schoschina, 1997). 

    Laminaria hyperborea has an optimum temperature for growth of 15°C, and an upper temperature limit of 21°C (Bolton & Lüning, 1982). At 17°C gamete survival is reduced (Steinhoff et al., 2008) and gametogenesis is inhibited at 21°C (Dieck, 1992). It is therefore likely that Laminaria hyperborea recruitment will be impaired at a sustained temperature increase of above 17°C. However, sporophytes can tolerate slightly higher temperatures of 20°C. Temperature tolerances for Laminaria hyperborea are also seasonally variable and temperature changes are less tolerated in winter months than summer months (Birkett et al., 1998b).

    There is evidence that climate change is already having an impact on Laminaria hyperborea populations in the English Channel. Poleward range expansion of the warm temperate Laminaria ochroleuca as a result of ocean warming has led to competition with Laminaria hyperborea in UK waters (Smale et al., 2015). Laminaria ochroleucawas not found in the UK last century.  But Laminaria ochroleuca has now increased its range to include the southwest of England (Smale et al., 2015) and the west coast of Ireland (Schoenrock et al., 2019). While, since 1970 Laminaria hyperborea has undergone a range constriction of ~250 km at its warm leading-edge (Frontier et al., 2021). 

    During the 2013-2014 Northeast Atlantic storm season, the UK was subjected to some of the most intense storms recorded within the past five years. A study by Smale & Vance. (2015) investigated the impacts of the storms on kelp canopies along the south coast of the UK, findings indicated monospecific canopies of Laminaria hyperborea were unaffected by the storms. However, the storms significantly altered a mixed canopy study site, composed of Laminaria ochroleuca, Saccharina latissima and Laminaria hyperborea. Therefore, if climate change continues to change species composition within kelp forests resistance to storm disturbance could be altered.

    Smale et al. (2015) found that Laminaria hyperborea suffered from much higher epiphytic loadings and lower productivity than its competitor Laminaria ochroleuca during the summer months, which reduced its competitive ability. The decreased competitive ability because of ocean warming corresponds to findings by Pessarrodona et al. (2018), who found a decrease in the size of Laminaria hyperborea plants along a north-south gradient in Scotland, with average maximum stipe lengths of over 150 cm, whereas in southern England they were less than 100 cm. Similarly, Smale et al. (2020b) observed clear differences between net primary productivity (NNP) and carbon standing stock of Laminaria hyperborea between the colder northern and warmer southern test sites in the UK, with NNP and standing stock being 1.5 and 2.5 times greater in the northern sites. Identifying ocean temperatures as a lively driver of productivity, with reduced NNP and standing stock observed in warmer waters (Smale et al., 2020b). 

    The decrease in productivity in southern England suggests that Laminaria hyperborea is already growing at suboptimal temperatures. Assis et al. (2018) predicted that under the highest emission scenario (RCP 8.5) the biogeographic range of Laminaria hyperborea will move northwards, and this retreat would lead to this species being lost from approximately 30% of the UK coastline.

    Subtidal red algae are less tolerant of temperature extremes than intertidal red algae, surviving between -2°C and 18-23°C (Lüning 1990; Kain & Norton, 1990). Temperature increases may affect growth, recruitment, or interfere with reproduction processes. For example, there is some evidence to suggest that blade growth in Delesseria sanguinea is delayed until ambient sea temperatures fall below 13°C.  Blade growth is also likely to be intrinsically linked to gametangia development (Kain, 1987), and maintenance of sea temperatures above 13°C may affect recruitment success.

    Sensitivity assessment. Laminaria hyperborea is already growing at suboptimal temperatures in the southern UK, based on evidence of its decreased productivity comparative to Scotland (Pessarrodona et al., 2018; Smale et al., 2020b), and predictions have estimated Laminaria hyperborea to be lost from the UK by 2100 as a result of warming (Brodie et al., 2014). Sea surface temperatures around the UK currently ranging from 6-19°C (Huthnance, 2010).  Under the middle emission scenario, a rise of 3°C could lead to maximum summer high temperatures in the south of the UK of 22°C. This is above the upper thermal limit of 21°C for Laminaria hyperborea (Bolton & Lüning, 1982), and is likely to lead to loss of this species from the south of England. Furthermore, biomass and plant size are expected to decrease as waters warm, with Scottish Laminaria hyperborea stipe lengths decreasing to lengths observed in southern England, leading to a decline in carbon assimilation, productivity and habitat quality. Therefore, resistance is assessed as ‘Medium’, and resilience is assessed as ‘Very Low’, as the loss is likely to be a long-term decline, due to the long-term nature of ocean warming. Therefore, this biotope is assessed as ‘Medium’ sensitivity to ocean warming under this scenario.

    For the high emission scenario and extreme scenario, this northward retreat of the distribution of Laminaria hyperborea is expected to increase. Under the high emission scenario it is expected to be lost from 30% of the coastline around the UK (Assis et al., 2018), and under the extreme scenario more is projected to be lost. Populations that remain around the UK will become less productive. Therefore, under these scenarios, resistance is assessed as ‘Low’, and resilience is assessed as ‘Very Low’. Therefore, this biotope IR.HIR.KFaR.LhypFa is assessed as ‘High’ sensitivity to ocean warming under this scenario.

    Low
    High
    High
    High
    Help
    Very Low
    High
    High
    High
    Help
    High
    High
    High
    High
    Help
    Global warming (middle) [Show more]

    Global warming (middle)

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

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

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

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

    Evidence

    The distribution of kelp is strongly influenced by climatic conditions; therefore, kelp species are extremely sensitive to the ongoing ocean warming (Kain, 1979; Van Den Hoek, 1982; Breeman, 1990; Lüning, 1990; Assis et al., 2016; Smale, 2020). Northern distribution boundaries are set by winter temperatures that are lethal, or summer temperatures too low for growth and/or reproduction, whilst southern limits are set by high lethal summer temperatures or winter temperatures too high for induction of a crucial step in the life cycle (Breeman, 1990). Kelps have a high dependence on ocean temperatures, which make them highly vulnerable to ocean warming (Assis et al., 2014). Laminaria hyperborea is a cold- temperate kelp species, distributed from the Barents Sea down to the coast of Portugal (Schoschina, 1997). 

    Laminaria hyperborea has an optimum temperature for growth of 15°C, and an upper temperature limit of 21°C (Bolton & Lüning, 1982). At 17°C gamete survival is reduced (Steinhoff et al., 2008) and gametogenesis is inhibited at 21°C (Dieck, 1992). It is therefore likely that Laminaria hyperborea recruitment will be impaired at a sustained temperature increase of above 17°C. However, sporophytes can tolerate slightly higher temperatures of 20°C. Temperature tolerances for Laminaria hyperborea are also seasonally variable and temperature changes are less tolerated in winter months than summer months (Birkett et al., 1998b).

    There is evidence that climate change is already having an impact on Laminaria hyperborea populations in the English Channel. Poleward range expansion of the warm temperate Laminaria ochroleuca as a result of ocean warming has led to competition with Laminaria hyperborea in UK waters (Smale et al., 2015). Laminaria ochroleucawas not found in the UK last century.  But Laminaria ochroleuca has now increased its range to include the southwest of England (Smale et al., 2015) and the west coast of Ireland (Schoenrock et al., 2019). While, since 1970 Laminaria hyperborea has undergone a range constriction of ~250 km at its warm leading-edge (Frontier et al., 2021). 

    During the 2013-2014 Northeast Atlantic storm season, the UK was subjected to some of the most intense storms recorded within the past five years. A study by Smale & Vance. (2015) investigated the impacts of the storms on kelp canopies along the south coast of the UK, findings indicated monospecific canopies of Laminaria hyperborea were unaffected by the storms. However, the storms significantly altered a mixed canopy study site, composed of Laminaria ochroleuca, Saccharina latissima and Laminaria hyperborea. Therefore, if climate change continues to change species composition within kelp forests resistance to storm disturbance could be altered.

    Smale et al. (2015) found that Laminaria hyperborea suffered from much higher epiphytic loadings and lower productivity than its competitor Laminaria ochroleuca during the summer months, which reduced its competitive ability. The decreased competitive ability because of ocean warming corresponds to findings by Pessarrodona et al. (2018), who found a decrease in the size of Laminaria hyperborea plants along a north-south gradient in Scotland, with average maximum stipe lengths of over 150 cm, whereas in southern England they were less than 100 cm. Similarly, Smale et al. (2020b) observed clear differences between net primary productivity (NNP) and carbon standing stock of Laminaria hyperborea between the colder northern and warmer southern test sites in the UK, with NNP and standing stock being 1.5 and 2.5 times greater in the northern sites. Identifying ocean temperatures as a lively driver of productivity, with reduced NNP and standing stock observed in warmer waters (Smale et al., 2020b). 

    The decrease in productivity in southern England suggests that Laminaria hyperborea is already growing at suboptimal temperatures. Assis et al. (2018) predicted that under the highest emission scenario (RCP 8.5) the biogeographic range of Laminaria hyperborea will move northwards, and this retreat would lead to this species being lost from approximately 30% of the UK coastline.

    Subtidal red algae are less tolerant of temperature extremes than intertidal red algae, surviving between -2°C and 18-23°C (Lüning 1990; Kain & Norton, 1990). Temperature increases may affect growth, recruitment, or interfere with reproduction processes. For example, there is some evidence to suggest that blade growth in Delesseria sanguinea is delayed until ambient sea temperatures fall below 13°C.  Blade growth is also likely to be intrinsically linked to gametangia development (Kain, 1987), and maintenance of sea temperatures above 13°C may affect recruitment success.

    Sensitivity assessment. Laminaria hyperborea is already growing at suboptimal temperatures in the southern UK, based on evidence of its decreased productivity comparative to Scotland (Pessarrodona et al., 2018; Smale et al., 2020b), and predictions have estimated Laminaria hyperborea to be lost from the UK by 2100 as a result of warming (Brodie et al., 2014). Sea surface temperatures around the UK currently ranging from 6-19°C (Huthnance, 2010).  Under the middle emission scenario, a rise of 3°C could lead to maximum summer high temperatures in the south of the UK of 22°C. This is above the upper thermal limit of 21°C for Laminaria hyperborea (Bolton & Lüning, 1982), and is likely to lead to loss of this species from the south of England. Furthermore, biomass and plant size are expected to decrease as waters warm, with Scottish Laminaria hyperborea stipe lengths decreasing to lengths observed in southern England, leading to a decline in carbon assimilation, productivity and habitat quality. Therefore, resistance is assessed as ‘Medium’, and resilience is assessed as ‘Very Low’, as the loss is likely to be a long-term decline, due to the long-term nature of ocean warming. Therefore, this biotope is assessed as ‘Medium’ sensitivity to ocean warming under this scenario.

    For the high emission scenario and extreme scenario, this northward retreat of the distribution of Laminaria hyperborea is expected to increase. Under the high emission scenario it is expected to be lost from 30% of the coastline around the UK (Assis et al., 2018), and under the extreme scenario more is projected to be lost. Populations that remain around the UK will become less productive. Therefore, under these scenarios, resistance is assessed as ‘Low’, and resilience is assessed as ‘Very Low’. Therefore, this biotope IR.HIR.KFaR.LhypFa is assessed as ‘High’ sensitivity to ocean warming under this scenario.

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

    Marine heatwaves (high)

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

    Evidence

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

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

    Under experimental conditions, Nepper-Davidson et al. (2019) exposed a northern (Denmark) population of Saccharina lattisima to a simulated three week heatwaves of three different intensities; 18, 21 and 24°C. When exposed to heatwaves of 18 and 21°C there was a decrease in photosynthesis and growth. When a 24°C was simulated, 91% of sporophytes were dead within a week, and the fronds of the few survivors were disintegrating, so the experiment was terminated (Nepper-Davidsen et al., 2019). 

    Laminaria hyperborea is a cold-temperate species of kelp with an optimum temperature for growth of 15°C, and an upper temperature limit of 21°C (Bolton & Lüning, 1982). Germination success can decrease by almost two thirds at temperatures as low as 17°C. Therefore it is expected that similar to other kelp species, Laminaria hyperborea will be highly sensitive to marine heatwaves.

    Sensitivity assessment. Under the middle emission scenario, if heatwaves occurred every three years, with a maximum intensity of 2°C for 80 days by the end of this century, this could lead to summer sea temperatures reaching up to 24°C in southern England. Laminaria hyperborea is unlikely to survive a heatwave of this magnitude and is, therefore, likely to suffer severe mortality in the south. In Scotland, where a significant portion of Laminaria hyperborea populations occur, temperatures are not predicted to rise above 20°C, and are, therefore,  Laminaria hyperborea is likely to survive a heatwave of this magnitude.  Therefore, resistance has been assessed as ‘Medium’. As a further heatwave (as defined by the pressure benchmark) is likely to affect this habitat before full recovery, resilience has been assessed as ‘Low.’ Therefore, this biotope IR.HIR.KFaR.LhypFa is assessed as having ‘Medium’ sensitivity to marine heatwaves under the middle emission scenario.

    Under the high emission scenario, if heatwaves occur every two years by the end of this century, reaching a maximum intensity of 3.5°C for 120 days, this could lead to the heatwave lasting the entire summer with temperatures reaching up to 26.5°C in southern England. Laminaria hyperborea is unlikely to survive a heatwave of this magnitude, and as temperatures are likely to reach >21°C in Scotland under this scenario, there is likely to be mortality throughout this species’ UK biogeographic distribution. Therefore, resistance has been assessed as ‘Low’. As a further heatwave is likely to affect this habitat before full recovery (under the pressure benchmark definition), resilience has been assessed as ‘Low.’ Therefore, this biotope IR.HIR.KFaR.LhypFa is assessed as having ‘High’ sensitivity to marine heatwaves under the high emission scenario.

    Low
    Medium
    Medium
    High
    Help
    Low
    High
    High
    High
    Help
    High
    Medium
    Medium
    High
    Help
    Marine heatwaves (middle) [Show more]

    Marine heatwaves (middle)

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

    Evidence

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

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

    Under experimental conditions, Nepper-Davidson et al. (2019) exposed a northern (Denmark) population of Saccharina lattisima to a simulated three week heatwaves of three different intensities; 18, 21 and 24°C. When exposed to heatwaves of 18 and 21°C there was a decrease in photosynthesis and growth. When a 24°C was simulated, 91% of sporophytes were dead within a week, and the fronds of the few survivors were disintegrating, so the experiment was terminated (Nepper-Davidsen et al., 2019). 

    Laminaria hyperborea is a cold-temperate species of kelp with an optimum temperature for growth of 15°C, and an upper temperature limit of 21°C (Bolton & Lüning, 1982). Germination success can decrease by almost two thirds at temperatures as low as 17°C. Therefore it is expected that similar to other kelp species, Laminaria hyperborea will be highly sensitive to marine heatwaves.

    Sensitivity assessment. Under the middle emission scenario, if heatwaves occurred every three years, with a maximum intensity of 2°C for 80 days by the end of this century, this could lead to summer sea temperatures reaching up to 24°C in southern England. Laminaria hyperborea is unlikely to survive a heatwave of this magnitude and is, therefore, likely to suffer severe mortality in the south. In Scotland, where a significant portion of Laminaria hyperborea populations occur, temperatures are not predicted to rise above 20°C, and are, therefore,  Laminaria hyperborea is likely to survive a heatwave of this magnitude.  Therefore, resistance has been assessed as ‘Medium’. As a further heatwave (as defined by the pressure benchmark) is likely to affect this habitat before full recovery, resilience has been assessed as ‘Low.’ Therefore, this biotope IR.HIR.KFaR.LhypFa is assessed as having ‘Medium’ sensitivity to marine heatwaves under the middle emission scenario.

    Under the high emission scenario, if heatwaves occur every two years by the end of this century, reaching a maximum intensity of 3.5°C for 120 days, this could lead to the heatwave lasting the entire summer with temperatures reaching up to 26.5°C in southern England. Laminaria hyperborea is unlikely to survive a heatwave of this magnitude, and as temperatures are likely to reach >21°C in Scotland under this scenario, there is likely to be mortality throughout this species’ UK biogeographic distribution. Therefore, resistance has been assessed as ‘Low’. As a further heatwave is likely to affect this habitat before full recovery (under the pressure benchmark definition), resilience has been assessed as ‘Low.’ Therefore, this biotope IR.HIR.KFaR.LhypFa is assessed as having ‘High’ sensitivity to marine heatwaves under the high emission scenario.

    Medium
    Medium
    Medium
    High
    Help
    Low
    High
    High
    High
    Help
    Medium
    Medium
    Medium
    High
    Help
    Ocean acidification (high) [Show more]

    Ocean acidification (high)

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

    Evidence

    Increasing levels of CO2 in the atmosphere have led to the average pH of sea surface waters dropping from 8.25 in the 1700s to 8.14 in the 1990s (Jacobson, 2005), with it expected to drop up to a further 0.35 units by the end of this century, dependent on emission scenario. Marine autotrophs will generally benefit from ocean acidification, through an increase in the availability of aqueous CO2 for photosynthesis (Koch et al., 2013).

    Most species of kelp, including Laminaria hyperborea, appear to be undersaturated in respect to carbon dioxide, although they can generally utilise HCO3 and have external carbonic anhydrase for extracellular dehydration of HCO3 to CO2 (Koch et al., 2013). This was confirmed for Laminaria hyperborea by Olischläger et al. (2012) who found that ocean acidification at levels expected for the end of this century (700 µatm CO2; a value between the middle and high emission scenario) led to an increase in female gametogenesis and increasing net photosynthesis and growth of sporophytes.

    Research on other kelp species has revealed a positive or neutral effect of ocean acidification (Roleda et al., 2012, Fernández et al., 2015, Nunes et al., 2015, Iñiguez et al., 2016b, a), except for one study, which found that ocean acidification negatively impacted photosynthesis and growth in the southern hemisphere species, Ecklonia radiata (Britton et al., 2016).

    Sensitivity assessment. Kelp forests live in a naturally variable pH habitat, with diel fluctuations of 0.3 - 0.45 pH units (Krause-Jensen et al., 2015, Britton et al., 2016), and boundary layer pH fluctuation of up to 0.8 units (Krause-Jensen et al., 2015). Laminaria hyperborea is not expected to be impacted by ocean acidification at levels expected for the end of this century. Therefore, under both the middle and high emission scenario resistance is assessed as ‘High’, and resilience is assessed as ‘High’ leading to a score of ‘Not sensitive’.

    High
    High
    Medium
    Medium
    Help
    High
    High
    High
    High
    Help
    Not sensitive
    High
    Medium
    Medium
    Help
    Ocean acidification (middle) [Show more]

    Ocean acidification (middle)

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

    Evidence

    Increasing levels of CO2 in the atmosphere have led to the average pH of sea surface waters dropping from 8.25 in the 1700s to 8.14 in the 1990s (Jacobson, 2005), with it expected to drop up to a further 0.35 units by the end of this century, dependent on emission scenario. Marine autotrophs will generally benefit from ocean acidification, through an increase in the availability of aqueous CO2 for photosynthesis (Koch et al., 2013).

    Most species of kelp, including Laminaria hyperborea, appear to be undersaturated in respect to carbon dioxide, although they can generally utilise HCO3 and have external carbonic anhydrase for extracellular dehydration of HCO3 to CO2 (Koch et al., 2013). This was confirmed for Laminaria hyperborea by Olischläger et al. (2012) who found that ocean acidification at levels expected for the end of this century (700 µatm CO2; a value between the middle and high emission scenario) led to an increase in female gametogenesis and increasing net photosynthesis and growth of sporophytes.

    Research on other kelp species has revealed a positive or neutral effect of ocean acidification (Roleda et al., 2012, Fernández et al., 2015, Nunes et al., 2015, Iñiguez et al., 2016b, a), except for one study, which found that ocean acidification negatively impacted photosynthesis and growth in the southern hemisphere species, Ecklonia radiata (Britton et al., 2016).

    Sensitivity assessment. Kelp forests live in a naturally variable pH habitat, with diel fluctuations of 0.3 - 0.45 pH units (Krause-Jensen et al., 2015, Britton et al., 2016), and boundary layer pH fluctuation of up to 0.8 units (Krause-Jensen et al., 2015). Laminaria hyperborea is not expected to be impacted by ocean acidification at levels expected for the end of this century. Therefore, under both the middle and high emission scenario resistance is assessed as ‘High’, and resilience is assessed as ‘High’ leading to a score of ‘Not sensitive’.

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

    Sea level rise (extreme)

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

    Evidence

    Sea-level rise is occurring through a combination of thermal expansion and ice melt.  Sea levels have risen 1-3 mm/yr. in the last century (Cazenave & Nerem, 2004, Church et al., 2004, Church & White, 2006). This biotope occurs on very exposed and exposed, but wave surged, upper infralittoral bedrock and massive boulders. Wave surge is reduced with increasing depth; therefore, sea-level rise may reduce the effect of wave surge in the deeper examples or deeper reaches of this biotope.

    The distribution of Laminaria hyperborea is positivity related to wave exposure, and as wave exposure increases, so does biomass and abundance (Pedersen et al., 2012). Total plant biomass and production per unit area double along an exposure gradient, due to larger leaf lengths and increased density at high wave energy sites (Pedersen et al., 2012). Understanding how sea-level rise will affect exposure and tidal energy is fraught with uncertainty, although evidence appears to suggest that any alterations will be non-linear (Pickering et al., 2012, Li et al., 2016). Modelling potential outcomes of sea-level rise on the tidal and residual currents in the Bohai Sea, China showed effects were site-dependent, with energy either increasing or decreasing (Li et al., 2016). Similarly, Pickering et al. (2012) found a similar pattern around the UK for tidal amplitude.

    Light availability and water turbidity are principle factors in determining kelp depth range (Birkett et al. 1998b), with laminarians being reported to be able to withstand light levels of up to 1% surface irradiance. An increase in depth due to sea-level rise is likely to impact both Laminaria hyperborea and any understory algae, negatively impacting this biotope. The most important factors explaining the distribution of Laminaria hyperborea along the Norwegian coast were depth, wave exposure, light exposure and topography (Bekkby et al., 2009). This species requires rocky substratum for attachment.

    Sensitivity assessment. This biotope IR.HIR.KFaR.LhypFa is recorded from 0-20 m in depth.  As wave surge diminishes with increased depth, sea-level rise is likely to lead to the density of faunal turf reducing at the deeper reaches of this biotope and transitioning into a biotope characterised by kelp and dense red seaweeds (IR.HIR.KFaR.LhypR.Ft or IR.HIR.KFaR.LhypR.Pk) or dense foliose red algae (IR.HIR.KFaR.FoR.Dic). This biotope may be able to expand its range and migrate landwards to compensate for sea-level rise, if not constrained by lack of suitable substrate or human-modified shorelines.

    There is likely to be considerable variation between sites, the relative contribution of wave surge and exposure to habitat suitability, and the depth range occupied by the biotope. Hence, it is difficult to assess the effect of the different sea-level rise scenarios. However, as the biotope can occur from 0-20 m in depth, it is assumed at a sea-level rise of 50 cm, or 70 cm (middle to high emission scenarios) would have limited effect but that a 107 cm rise (the extreme emission scenario) might result in loss of some of the deeper extent of the biotope in some sites. Therefore, resistance is assessed as ‘High’ under the middle and high emission scenarios so that resilience is ‘High’ and sensitivity assessed as ‘Not sensitive’. But resistance is possibly ‘Medium’ under the extreme emission scenario so that resilience is ‘Very low’ and sensitivity assessed as ‘Medium’, albeit with ‘Low’ confidence.

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

    Sea level rise (high)

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

    Evidence

    Sea-level rise is occurring through a combination of thermal expansion and ice melt.  Sea levels have risen 1-3 mm/yr. in the last century (Cazenave & Nerem, 2004, Church et al., 2004, Church & White, 2006). This biotope occurs on very exposed and exposed, but wave surged, upper infralittoral bedrock and massive boulders. Wave surge is reduced with increasing depth; therefore, sea-level rise may reduce the effect of wave surge in the deeper examples or deeper reaches of this biotope.

    The distribution of Laminaria hyperborea is positivity related to wave exposure, and as wave exposure increases, so does biomass and abundance (Pedersen et al., 2012). Total plant biomass and production per unit area double along an exposure gradient, due to larger leaf lengths and increased density at high wave energy sites (Pedersen et al., 2012). Understanding how sea-level rise will affect exposure and tidal energy is fraught with uncertainty, although evidence appears to suggest that any alterations will be non-linear (Pickering et al., 2012, Li et al., 2016). Modelling potential outcomes of sea-level rise on the tidal and residual currents in the Bohai Sea, China showed effects were site-dependent, with energy either increasing or decreasing (Li et al., 2016). Similarly, Pickering et al. (2012) found a similar pattern around the UK for tidal amplitude.

    Light availability and water turbidity are principle factors in determining kelp depth range (Birkett et al. 1998b), with laminarians being reported to be able to withstand light levels of up to 1% surface irradiance. An increase in depth due to sea-level rise is likely to impact both Laminaria hyperborea and any understory algae, negatively impacting this biotope. The most important factors explaining the distribution of Laminaria hyperborea along the Norwegian coast were depth, wave exposure, light exposure and topography (Bekkby et al., 2009). This species requires rocky substratum for attachment.

    Sensitivity assessment. This biotope IR.HIR.KFaR.LhypFa is recorded from 0-20 m in depth.  As wave surge diminishes with increased depth, sea-level rise is likely to lead to the density of faunal turf reducing at the deeper reaches of this biotope and transitioning into a biotope characterised by kelp and dense red seaweeds (IR.HIR.KFaR.LhypR.Ft or IR.HIR.KFaR.LhypR.Pk) or dense foliose red algae (IR.HIR.KFaR.FoR.Dic). This biotope may be able to expand its range and migrate landwards to compensate for sea-level rise, if not constrained by lack of suitable substrate or human-modified shorelines.

    There is likely to be considerable variation between sites, the relative contribution of wave surge and exposure to habitat suitability, and the depth range occupied by the biotope. Hence, it is difficult to assess the effect of the different sea-level rise scenarios. However, as the biotope can occur from 0-20 m in depth, it is assumed at a sea-level rise of 50 cm, or 70 cm (middle to high emission scenarios) would have limited effect but that a 107 cm rise (the extreme emission scenario) might result in loss of some of the deeper extent of the biotope in some sites. Therefore, resistance is assessed as ‘High’ under the middle and high emission scenarios so that resilience is ‘High’ and sensitivity assessed as ‘Not sensitive’. But resistance is possibly ‘Medium’ under the extreme emission scenario so that resilience is ‘Very low’ and sensitivity assessed as ‘Medium’, albeit with ‘Low’ confidence.

    High
    Low
    NR
    NR
    Help
    High
    High
    High
    High
    Help
    Not sensitive
    Low
    Low
    Low
    Help
    Sea level rise (middle) [Show more]

    Sea level rise (middle)

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

    Evidence

    Sea-level rise is occurring through a combination of thermal expansion and ice melt.  Sea levels have risen 1-3 mm/yr. in the last century (Cazenave & Nerem, 2004, Church et al., 2004, Church & White, 2006). This biotope occurs on very exposed and exposed, but wave surged, upper infralittoral bedrock and massive boulders. Wave surge is reduced with increasing depth; therefore, sea-level rise may reduce the effect of wave surge in the deeper examples or deeper reaches of this biotope.

    The distribution of Laminaria hyperborea is positivity related to wave exposure, and as wave exposure increases, so does biomass and abundance (Pedersen et al., 2012). Total plant biomass and production per unit area double along an exposure gradient, due to larger leaf lengths and increased density at high wave energy sites (Pedersen et al., 2012). Understanding how sea-level rise will affect exposure and tidal energy is fraught with uncertainty, although evidence appears to suggest that any alterations will be non-linear (Pickering et al., 2012, Li et al., 2016). Modelling potential outcomes of sea-level rise on the tidal and residual currents in the Bohai Sea, China showed effects were site-dependent, with energy either increasing or decreasing (Li et al., 2016). Similarly, Pickering et al. (2012) found a similar pattern around the UK for tidal amplitude.

    Light availability and water turbidity are principle factors in determining kelp depth range (Birkett et al. 1998b), with laminarians being reported to be able to withstand light levels of up to 1% surface irradiance. An increase in depth due to sea-level rise is likely to impact both Laminaria hyperborea and any understory algae, negatively impacting this biotope. The most important factors explaining the distribution of Laminaria hyperborea along the Norwegian coast were depth, wave exposure, light exposure and topography (Bekkby et al., 2009). This species requires rocky substratum for attachment.

    Sensitivity assessment. This biotope IR.HIR.KFaR.LhypFa is recorded from 0-20 m in depth.  As wave surge diminishes with increased depth, sea-level rise is likely to lead to the density of faunal turf reducing at the deeper reaches of this biotope and transitioning into a biotope characterised by kelp and dense red seaweeds (IR.HIR.KFaR.LhypR.Ft or IR.HIR.KFaR.LhypR.Pk) or dense foliose red algae (IR.HIR.KFaR.FoR.Dic). This biotope may be able to expand its range and migrate landwards to compensate for sea-level rise, if not constrained by lack of suitable substrate or human-modified shorelines.

    There is likely to be considerable variation between sites, the relative contribution of wave surge and exposure to habitat suitability, and the depth range occupied by the biotope. Hence, it is difficult to assess the effect of the different sea-level rise scenarios. However, as the biotope can occur from 0-20 m in depth, it is assumed at a sea-level rise of 50 cm, or 70 cm (middle to high emission scenarios) would have limited effect but that a 107 cm rise (the extreme emission scenario) might result in loss of some of the deeper extent of the biotope in some sites. Therefore, resistance is assessed as ‘High’ under the middle and high emission scenarios so that resilience is ‘High’ and sensitivity assessed as ‘Not sensitive’. But resistance is possibly ‘Medium’ under the extreme emission scenario so that resilience is ‘Very low’ and sensitivity assessed as ‘Medium’, albeit with ‘Low’ confidence.

    High
    Low
    NR
    NR
    Help
    High
    High
    High
    High
    Help
    Not sensitive
    Low
    Low
    Low
    Help

    Hydrological Pressures

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

    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

    Kain (1964) stated that Laminaria hyperborea sporophyte growth and reproduction could occur within a temperature range of 0 - 20°C. Upper and lower lethal temperatures have been estimated at between 1-2°C above or below the extremes of this range (Birkett et al., 1988). Above 17°C gamete survival is reduced (Kain, 1964 & 1971) and gametogenesis is inhibited at 21°C (Dieck, 1992). It is therefore likely that Laminaria hyperborea recruitment will be impaired at a sustained temperature increase of above 17°C. Sporophytes however can tolerate slightly higher temperatures of 20°C. Temperature tolerances for Laminaria hyperborea are also seasonally variable and temperature changes are less tolerated in winter months than summer months (Birkett et al., 1998).

    Subtidal red algae are less tolerant of temperature extremes than intertidal red algae, surviving between -2°C and 18-23°C (Lüning 1990; Kain & Norton, 1990).  Temperature increase may affect growth, recruitment or interfere with reproduction processes. For example, there is some evidence to suggest that blade growth in Delesseria sanguinea is delayed until ambient sea temperatures fall below 13°C. Blade growth is also likely to be intrinsically linked to gametangia development (Kain, 1987), and maintenance of sea temperatures above 13°C may affect recruitment success.

    Sensitivity assessment. This biotope is distributed throughout the UK (Connor et al., 2004). Northern to southern Sea Surface Temperature (SST) ranges from 8-16°C in summer and 6-13°C in winter (Beszczynska-Möller & Dye, 2013). Overall, a chronic change (2°C for a year) outside normal range for a year may reduce recruitment and growth, resulting in a minor loss in the population of kelp, especially in winter months or in southern examples of the biotope. However, an acute change (5°C for a month; e.g. from thermal effluent) may result in loss of abundance of kelp or extent of the bed, especially in winter. Therefore, resistance to the pressure is considered 'Medium', and resilience 'Medium'. The sensitivity of this biotope to increases in temperature has been assessed as 'Medium'.

    Medium
    High
    High
    High
    Help
    Medium
    High
    High
    High
    Help
    Medium
    High
    High
    High
    Help
    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

    Kain (1964) stated that Laminaria hyperborea sporophyte growth and reproduction could occur within a temperature range of 0 - 20°C. Upper and lower lethal temperatures have been estimated at between 1-2 °C above or below the extremes of this range (Birkett et al., 1988). Subtidal red algae can survive at temperatures between -2 °C and 18-23 °C (Lüning, 1990; Kain & Norton, 1990).

    Laminaria hyperborea is a boreal northern species with a geographic range from mid Portugal to Northern Norway (Birket et al., 1998), and a mid range within southern Norway (60°-65° North)(Kain, 1971). The average seawater temperature for southern Norway in October is 12-13°C (Miller et al., 2009), and average annual sea temperature, from 1970-2014, is 8°C (Beszczynska-Möller & Dye, 2013). The available information suggests that Laminaria hyperborea and biotope structure would not be affected by a change in sea temperature at the benchmark level.

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

     

    High
    High
    High
    High
    Help
    High
    High
    High
    High
    Help
    Not sensitive
    High
    High
    High
    Help
    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. Birkett et al, (1998) suggested that long-term increases in salinity may affect Laminaria hyperborea growth and may result in loss of affected kelp, and therefore loss of the biotope.

    Sensitivity assessment. Resistance to the pressure is considered ‘Low’, and resilience ‘Medium’.  The sensitivity of this biotope to an increase in salinity has been assessed as ‘Medium’.

    Low
    Low
    NR
    NR
    Help
    Medium
    High
    Medium
    High
    Help
    Medium
    Low
    NR
    NR
    Help
    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. Birkett et al,. (1998) suggest that long-term changes in salinity may result in loss of affected kelp and, therefore loss of this biotope.

    Hopkin & Kain (1978) tested Laminaria hyperborea sporophyte growth at various low salinity treatments. The results showed that Laminaria hyperborea sporophytes could grow “normally” at 19 psu, growth was reduced at 16 psu and did not grow at 7 psu. A decrease in one MNCR salinity scale from 'Full' salinity (30-40psu) to 'Reduced' salinity (18-30 psu) would result in a decrease of Laminaria hyperborea sporophyte growth. Laminaria hyperborea may also be out-competed by low salinity tolerant species e.g. Saccharina latissma (Karsten, 2007), or the Invasive Non Indigenous Species Undaria pinnatifida (Burrows et al., 2014).

    If salinity was returned to 'Full' salinity (30-40 psu) Laminaria hyperborea could out-compete Saccharina latissma and re-establish community dominance in 2-4 years (Kain, 1975; Leinaas & Christie, 1996), however full habitat structure may take over 10 years to recover (Birkett et al., 1998; Cristie et al., 1998). The ability of Laminaria hyperborea to out-compete Undaria pinnatifida within the UK is however unknown (Heiser et al., 2014), and as such interspecific interaction between Laminaria hyperborea and Undaria pinnatifida is not included within this sensitivity assessment.

    Sensitivity assessment. Resistance to the pressure is considered ‘Low’, and resilience ‘Medium’.  The sensitivity of this biotope to decreases in salinity has been assessed as ‘Medium’.

    Low
    Medium
    Medium
    Medium
    Help
    Medium
    High
    Medium
    High
    Help
    Medium
    Medium
    Medium
    Medium
    Help
    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

    Kregting et al. (2013) measured Laminaria hyperborea blade growth and stipe elongation from an exposed and a sheltered site in Strangford Lough, Ireland, from March 2009-April 2010. Maximal significant wave height (Hm0) was 3.67 & 2m at the exposed and sheltered sites, and maximal water velocity (Velrms) was 0.6 & 0.3m/s at the exposed and sheltered sites respectively. Despite the differences in wave exposure and water velocity there was no significant difference in Laminaria hyperborea growth between the exposed and sheltered sites. Therefore water flow was found to have no significant effect on Laminaria hyperborea growth at the observed range of water velocities.

    Biotope structure is however different between wave exposed and sheltered sites. Pedersen et al. (2012) observed Laminaria hyperborea biomass, productivity and density increased with an increase in wave exposure. At low wave exposure Laminaria hyperborea canopy forming plants were smaller, had lower densities and had higher mortality rates than at exposed sites. At low wave exposure Pedersen et al. (2012) suggested that high epiphytic loading on Laminaria hyperborea impaired light conditions, nutrient uptake, and increased the drag on the host Laminaria hyperborea during extreme storm events.

    The morphology of the stipe and blade of kelps vary with water flow.  In wave exposed areas, for example, Laminaria hyperborea develops a long and flexible stipe and this is probably a functional adaptation to strong water movement (Sjøtun, 1998). In addition, the lamina becomes narrower and thinner in strong currents (Sjøtun & Fredriksen, 1995). However, the stipe of Laminaria hyperborea is relatively stiff and can snap in strong currents. Laminaria hyperborea is usually absent from areas of high wave action or strong currents, although it is found  in the Menai Strait, Wales, where tidal velocities can exceed 4 m/s (NBN, 2015) and in tidal rapids in Norway (J. Jones, pers. comm.)  Laminaria hyperborea growth can persist in very strong tidal streams (>3 m/s).

    Increase water flow rate may also remove or inhibit grazers including Patella pellucida and Echinus esculentus and remove epiphytic algae growth (Pedersen et al., 2012). The associated algal flora and suspension feeding faunal populations change significantly with different water flow regimes. Increased water flow rates may reduce the understorey epiflora, to be replaced by an epifauna dominated community (e.g. sponges, anemones and polyclinid ascidians) as in the biotope IR.HIR.KFaR.LhypFa. The composition of the holdfast fauna may also change, e.g. energetic or sheltered water movements favour different species of amphipods (Moore, 1985).

    IR.HIR.KFaR.LhypR, IR.HIR.KFaR.LhypFa, IR.MIR.KR.Lhyp, and their associated sub-biotopes are found within strong (1.5-3 m/s)-moderate (0.5-1.5 m/s) tidal streams. A change in peak mean spring bed flow velocity which does not result in a change in tidal streams above or below 0.5-3 m/s is not likely to affect the dominance of Laminaria hyperborea within the community, but may cause changes in the understorey community. The prominent understorey filter feeding community within IR.HIR.KFaR.LhypFa is reliant on high water movement. A decrease in tidal streams may result in a decline of filter feeding fauna and an increase in red seaweeds within the understorey community or vice versa with an increase in tidal streams A decrease in tidal flow within this range may also decrease urchin dislodgment and increase urchin grazing. An increase in urchin grazing may cause a decline in the understorey community abundance and diversity (as in IR.MIR.KR.Lhyp.GzFt/Pk and IR.MIR.KR.LhypPar).

    Sensitivity assessment. A change in peak mean spring bed flow velocity of between 0.1m/s to 0.2m/s for more than 1 year is not likely to affect the dominance of Laminaria hyperborea, however subtle differences in tidal regime may influence the understorey community. Resistance to the pressure is considered ‘High’, and resilience ‘High’. Hence, the sensitivity of this biotope to changes in peak mean spring bed velocity has been assessed as ‘Not Sensitive’.

     

    However, if peak mean spring bed flow velocity changes but remains within 0.5-3 m/s Laminaria hyperborea is likely to remain the dominant habitat but the understorey community may be affected; directly by a change in water velocity or through increased grazing pressure.

    High
    High
    High
    High
    Help
    High
    High
    High
    High
    Help
    Not sensitive
    High
    High
    High
    Help
    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

    The upper limit of the Laminaria hyperborea bed is determined by wave action and water flow, desiccation, and competition from the more emergence resistant Laminaria digitata. Laminaria hyperborea exposed at extreme low water are very intolerant of desiccation, the most noticeable effect being bleaching of the frond and subsequent death of the meristem and loss of the plant. An increase in wave exposure (see below- water flow), as a result of increased emergence, has been found to exclude Laminaria hyperborea from shallow waters due to dislodgement of the sporophyte or snapping of the stipe (Birket et al., 1998). Hence, an increase in emergence is likely to lead to mortality of exposed Laminaria hyperborea and the associated habitat.

    An increase in water depth/decreased emergence (at the benchmark level) may increase the upper depth restriction of Laminaria hyperborea forest biotope variants. However, limited light availability at depth will decrease the lower extent of Laminaria hyperborea, and may therefore result in a shift from forest to park biotope variants at depth. Further increases in depth will cause a community shift to that characterized by circalittoral faunal species, however this is beyond the scope of the benchmark.

    Sensitivity assessment. Resistance to the pressure is considered ‘Low’, and resilience ‘Medium’. The sensitivity of this biotope to changes in tidal emergence has been assessed as ‘Medium’.

    Low
    Low
    NR
    NR
    Help
    Medium
    High
    Low
    High
    Help
    Medium
    Low
    NR
    NR
    Help
    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

    Kregting et al., (2013) measured Laminaria hyperborea blade growth and stipe elongation from an exposed and a sheltered site in Strangford Lough, Ireland from March 2009-April 2010. Wave exposure was found to be between 1.1. to 1.6 times greater between the exposed and sheltered sites. Maximal significant wave height (Hm0) was 3.67 & 2m at the exposed and sheltered sites. Maximal water velocity (Velrms) was 0.6 & 0.3m/s at the exposed and sheltered sites. Despite the differences in wave exposure and water velocity there was no significant difference in Laminaria hyperborea growth between the exposed and sheltered site.

    Biotope structure is however different between wave exposed and sheltered sites. Pedersen et al., (2012) observed Laminaria hyperborea biomass, productivity and density increased with an increase in wave exposure. At low wave exposure Laminaria hyperborea canopy forming plants were smaller, had lower densities and had higher mortality rates than at exposed sites. At low wave exposure high epiphytic loading on Laminaria hyperborea was theorised to impair light conditions, nutrient uptake, and increase the drag of the host Laminaria hyperborea during extreme storm events.

    The morphology of the stipe and blade of kelps vary with water flow. In wave exposed areas, for example, Laminaria hyperborea develops a long and flexible stipe and this is probably a functional adaptation to strong water movement (Sjøtun, 1998). In addition, the lamina becomes narrower and thinner in strong currents (Sjøtun & Fredriksen, 1995). However, the stipe of Laminaria hyperborea is relatively stiff and can snap in strong currents. Lamiaria hyperborea is usually absent from areas of extreme wave action and can be replaced by Alaria esculenta. In extreme wave exposures Alaria esculenta can dominate the shallow sub-littoral to a depth of 15m (Birket et al., 1998).

    Increase water flow rate may also remove or inhibit grazers including Patella pellucida and Echinus esculentus and remove epiphytic algae growth (Pedersen et al., 2012). The associated algal flora and suspension feeding faunal populations change significantly with different water flow regimes. Increased water flow rates may reduce the understorey epiflora, to be replaced by an epifauna dominated community (e.g. sponges, anemones and polyclinid ascidians) as in the biotope IR.HIR.KFaR.LhypFa. The composition of the holdfast fauna may also change, e.g. energetic or sheltered water movements favour different species of amphipods (Moore, 1985).

    IR.HIR.KFaR.LhypR, IR.HIR.KFaR.LhypFa, IR.MIR.KR.Lhyp, and their associated sub-biotopes are found between extremely exposed to moderate wave exposure. Changes in local wave height above or below that experienced in extremely exposed to moderately exposed sites will affect the dominance of Laminaria hyperborea. Smaller changes in local wave height have the potential to cause changes to the understorey community. The prominent understorey filter feeding community within IR.HIR.KFaR.LhypFa is reliant on wave surge currents. A decrease in wave surge may result in a decline of filter feeding fauna and an increase in red seaweeds within the understorey community or vice versa. A decrease in local wave height may also decrease the chance of urchins being dislodged (removed) from biotopes found at sites with traditionally high wave exposure and may therefore increase urchin grazing. An increase in urchin grazing may cause a decline in the understorey community abundance and diversity (as in IR.MIR.KR.Lhyp.GzFt/Pk and IR.MIR.KR.LhypPar).

    Sensitivity assessment. A change in nearshore significant wave height >3% but <5% is however unlikely to have a significant effect. Resistance to the pressure is considered ‘High’, and resilience ‘High’. Hence, the sensitivity of this biotope to changes in local wave height has been assessed as ‘Not Sensitive’.

    High
    High
    High
    High
    Help
    High
    High
    High
    High
    Help
    Not sensitive
    High
    High
    High
    Help

    Chemical Pressures

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

    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.

    Bryan (1984) suggested that the general order for heavy metal toxicity in seaweeds is: Organic Hg > inorganic Hg > Cu > Ag > Zn > Cd > Pb. Cole et a,. (1999) reported that Hg was very toxic to macrophytes. Similarly, Hopkin & Kain (1978) demonstrated sub-lethal effects of heavy metals on Laminaria hyperborea gametophytes and sporophytes, including reduced growth and respiration. Sheppard et al., (1980) noted that increasing levels of heavy metal contamination along the west coast of Britain reduced species number and richness in holdfast fauna, except for suspension feeders which became increasingly dominant. Gastropods may be relatively tolerant of heavy metal pollution (Bryan, 1984). Echinus esculentus recruitment is likely to be impaired by heavy metal contamination due to the intolerance of its larvae. Echinus esculentus are long-lived and poor recruitment may not reduce grazing pressure in the short-term. Although macroalgae species may not be killed, except by high levels of contamination, reduced growth rates may impair the ability of the biotope to recover from other environmental disturbances.

    Not Assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    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.

    Laminaria hyperborea fronds, being almost exclusively sub tidal, would not come into contact with freshly released oil, but only to sinking emulsified oil and oil adsorbed onto particles (Birket et al., 1998). The mucilaginous slime layer coating of laminarians may protect them from smothering by oil. Hydrocarbons in solution reduce photosynthesis and may be algicidal. However, Holt et al,. (1995) reported that oil spills in the USA and from the 'Torrey Canyon' had little effect on kelp forests. Similarly, surveys of subtidal communities at a number sites between 1-22.5m below chart datum, including Laminaria hyperbora communities, showed no noticeable impacts of the Sea Empress oil spill and clean up (Rostron & Bunker, 1997). An assessment of holdfast fauna in Laminaria showed that although species richness and diversity decreased with increasing proximity to the Sea Empress oil spill, overall the holdfasts contained a reasonably rich and diverse fauna, even though oil was present in most samples (Sommerfield & Warwick, 1999). Laboratory studies of the effects of oil and dispersants on several red algae species, including Delesseria sanguinea (Grandy 1984; cited in Holt et al., 1995) concluded that they were all sensitive to oil/ dispersant mixtures, with little differences between adults, sporelings, diploid or haploid life stages. Holt et al., (1995) concluded that Delesseria sanguinea is probably generally sensitive of chemical contamination. Overall the red algae are likely to be highly intolerant to hydrocarbon contamination. Loss of red algae is likely to reduce the species richness and diversity of the biotope and the understorey may become dominated by encrusting corallines; however, red algae are likely to recover relatively quickly.

    Not Assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    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.

    O'Brian & Dixon (1976) suggested that red algae were the most sensitive group of macrophytes to oil and dispersant contamination (see Smith, 1968). Although Laminaria hyperborea sporelings and gametophytes are intolerant of atrazine (and probably other herbicides) overall they may be relatively tolerant of synthetic chemicals (Holt et al., 1995). Laminaria hyperborea survived within >55m from the acidified halogenated effluent discharge polluting Amlwch Bay, Anglesey, albeit at low density. These specimens were greater than 5 years of age, suggesting that spores and/or early stages were more intolerant (Hoare & Hiscock, 1974). Patella pellucida was excluded from Amlwch Bay by the pollution and the species richness of the holdfast fauna decreased with proximity to the effluent discharge; amphipods were particularly intolerant although polychaetes were the least affected (Hoare & Hiscock, 1974). The richness of epifauna/flora decreased near the source of the effluent and epiphytes were absent from Laminaria hyperborea stipes within Amlwch Bay. The red alga Phyllophora membranifolia was also tolerant of the effluent in Amlwch Bay. Smith (1968) also noted that epiphytic and benthic red algae were intolerant of dispersant or oil contamination due to the Torrey Canyon oil spill; only the epiphytes Crytopleura ramosa and Spermothamnion repens and some tufts of Jania rubens survived together with Osmundea pinnatifida, Gigartina pistillata and Phyllophora crispa from the sublittoral fringe. Delesseria sanguinea was probably to most intolerant since it was damaged at depths of 6m (Smith, 1968). Holt et al., (1995) suggested that Delesseria sanguinea is probably generally sensitive of chemical contamination. Although Laminaria hyperborea may be relatively insensitive to synthetic chemical pollution, evidence suggests that grazing gastropods, amphipods and red algae are sensitive. Loss of red algae is likely to reduce the species richness and diversity of the biotope and the understorey may become dominated by encrusting corallines; however, red algae are likely to recover relatively quickly.

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

    Radionuclide contamination

    Benchmark. An increase in 10µGy/h above background levels. 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 of other substances [Show more]

    Introduction of other substances

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

    Evidence

    This pressure is Not assessed.

    Not Assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    Not assessed (NA)
    NR
    NR
    NR
    Help
    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 inhibiting both photosynthesis and respiration in macroalgae (Kinne, 1977). Despite this, macroalgae are thought to buffer the environmental conditions of low oxygen, thereby acting as a refuge for organisms in oxygen depleted regions especially if the oxygen depletion is short-term (Frieder et al., 2012).  A rapid recovery from a state of low oxygen is expected if the environmental conditions are transient. If levels do drop below 4 mg/l negative effects on these organisms can be expected with adverse effects occurring below 2mg/l (Cole et al., 1999).

    Sensitivity Assessment. Reduced oxygen levels are likely to inhibit photosynthesis and respiration but not cause a loss of the macroalgae population directly.  However, small invertebrate epifauna may be lost, causing a reduction in species richness. Therefore a resistance of ‘High’ is recorded.  Resilience is likely to be ‘High’, and the biotopes is probably ‘Not sensitive’ at the benchmark level.

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

    Nutrient enrichment

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

    Evidence

    Holt et al. (1995) suggest that Laminaria hyperborea may be tolerant of nutrient enrichment since healthy populations are found at ends of sublittoral untreated sewage outfalls in the Isle of Man. Increased nutrient levels e.g. from sewage outfalls, has been associated with increases in abundance, primary biomass and Laminaria hyperborea stipe production but with concomitant decreases in species numbers and diversity (Fletcher, 1996).

    Increased nutrients may result in phytoplankton blooms that increase turbidity (see above). Increased nutrients may favour sea urchins, e.g. Echinus esculentus, due their ability to absorb dissolved organics, and result in increased grazing pressure leading to loss of understorey epiflora/fauna, decreased kelp recruitment and possibly 'urchin barrens'. Therefore, although nutrients may not affect kelps directly, indirect effects such as turbidity, siltation and competition may significantly affect the structure of the biotope.

    However this biotope is considered to be 'Not sensitive' at the pressure benchmark, that assumes compliance with good status as defined by the WFD.

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

    Organic enrichment

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

    Evidence

    Holt et al. (1995) suggest that Laminaria hyperborea may be tolerant of organic enrichment since healthy populations are found at ends of sub littoral untreated sewage outfalls in the Isle of Man. Increased nutrient levels e.g. from sewage outfalls, has been associated with increases in abundance, primary biomass and Laminaria hyperborea stipe production but with concomitant decreases in species numbers and diversity (Fletcher, 1996). Increase in ephemeral and opportunistic algae are associated with reduced numbers of perennial macrophytes (Fletcher, 1996). Increased nutrients may also result in phytoplankton blooms that increase turbidity. Therefore, although nutrients may not affect kelps directly, indirect effects such as turbidity may significantly affect the structure of Laminaria hyperborea biotopes.

    Sensitivity assessment. Resistance to the pressure is considered 'Medium', and resilience 'High'. The sensitivity of this biotope to organic enrichment is assessed as 'Low'.

    Medium
    Medium
    Medium
    Medium
    Help
    High
    High
    Medium
    High
    Help
    Low
    Medium
    Medium
    Medium
    Help

    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
    Help
    Very Low
    High
    High
    High
    Help
    High
    High
    High
    High
    Help
    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 Laminaria hyperborea would not be able to tolerate (Birket 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 sedimentary or soft rock substrata to hard rock or artificial substrata or vice-versa is assessed as “High”.

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

    Physical change (to another sediment type)

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

    Evidence

    Not relevant

    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    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 rock substrata.

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

    Christie et al., (1998) observed Laminaria hyperborea habitat regeneration following commercial Laminaria hyperborea trawling in south Norway. Within the study area, trawling removed all large canopy-forming adult Laminaria hyperborea, however sub-canopy recruits were largely unaffected. In 2-6 years of harvesting a new canopy had formed 1m off the seabed. The associated holdfast communities recovered in 6 years, however the epiphytic stipe community did not fully recover within the same time period. Christie et al., (1998) suggested that kelp habitats were relatively resistant to direct disturbance/removal of Laminaria hyperborea canopy.

    Recurrent disturbance occurring at a smaller time scale than the recovery period of 2-6 years (stated above) could extend recovery time. Kain (1975) cleared sublittoral blocks of Laminaria hyperborea at different times of the year for several years. The first colonizers and succession community differed between blocks and at what time of year the blocks were cleared however within 2 years of clearance the blocks were dominated by Laminaria hyperborea. Leinaas & Christie (1996) also observed Laminaria hyperborea re-colonization of “urchin barrens”, following removal of urchins. The substratum was initially colonized by filamentous macroalgae and Saccharina latissima however after 2-4 years Laminaria hyperborea dominated the community.

    Sensitivity assessment. Resistance to the pressure is considered ‘Low’, and resilience ‘Medium’. The sensitivity of this biotope to damage to seabed surface features is assessed as ‘Medium’.

     

    Low
    High
    High
    High
    Help
    Medium
    High
    High
    High
    Help
    Medium
    High
    High
    High
    Help
    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, please refer to pressure “Abrasion/disturbance of the substrata on the surface of the seabed”.

    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    Not relevant (NR)
    NR
    NR
    NR
    Help
    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). An increase in SPM results in a decrease in sub-surface light attenuation. Light availability and water turbidity are principal factors in determining kelp depth range (Birkett et al., 1998). Light penetration influences the maximum depth at which kelp species can grow and it has been reported that laminarians grow down to depths at which the light levels are reduced to 1 percent of incident light at the surface. Maximal depth distribution of laminarians, therefore, varies from 100 m in the Mediterranean to only 6-7 m in the silt-laden German Bight. In Atlantic European waters, the depth limit is typically 35 m. In very turbid waters the depth at which Laminaria hyperborea is found may be reduced, or in some cases excluded completely (e.g. Severn Estuary), because of the alteration in light attenuation by suspended sediment (Birkett et al. 1998b; Lüning, 1990).

    Laminaria spp. show a decrease of 50% photosynthetic activity when turbidity increases by 0.1/m (light attenuation coefficient =0.1-0.2/m; Staehr & Wernberg, 2009). An increase in water turbidity will likely affect the photosynthetic ability of Laminaria hyperborea and Laminaria ochroleuca and decrease Laminaria hyperborea abundance and density (see sub-biotope- IR.MIR.KR.Lhyp.Pk). Kain (1964) suggested that early Laminaria hyperborea gametophyte development could occur in the absence of light. Furthermore, observations from south Norway found that a pool of Laminaria hyperborea recruits could persist growing beneath Laminaria hyperborea canopies for several years, indicating that sporophyte growth can occur in light-limited environments (Christe et al., 1998). However in habitats exposed to high levels of suspended silts Laminaria hyperborea is out-competed by Saccharina latissima, a silt tolerant species, and thus, a decrease in water clarity is likely to decrease the abundance of Laminaria hyperborea in the affected area (Norton, 1978).

    Sensitivity Assessment. Changes in water clarity are likely to affect photosynthetic rates and enable Saccharina latissima to compete more successfully with Laminaria hyperborea.  A decrease in turbidity is likely to support enhanced growth (and possible habitat expansion) and is therefore not considered in this assessment.  An increase in water clarity from clear to intermediate (10-100 mg/l) represents a change in light attenuation of ca 0.67-6.7 Kd/m, and is likely to result in a greater than 50% reduction in photosynthesis of Laminaria spp. Therefore, the dominant kelp species will probably suffer a significant decline and resistance to this pressure is assessed as ‘Low’. Resilience to this pressure is probably ‘Medium’ at the benchmark.  Hence, this biotope is assessed as having a sensitivity of ‘Medium ‘to this pressure.

    Low
    High
    High
    High
    Help
    Medium
    High
    High
    High
    Help
    Medium
    High
    High
    High
    Help
    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

    Smothering by sediment e.g. 5 cm material during a discrete event, is unlikely to damage Laminaria hyperborea sporophytes but is likely to affect gametophyte survival as well as holdfast fauna, and interfere with zoospore settlement.  Given the microscopic size of the gametophyte, 5 cm of sediment could be expected to significantly inhibit growth. However, laboratory studies showed that gametophytes can survive in darkness for between 6 - 16 months at 8 °C and would probably survive smothering by a discrete event.  Once returned to normal conditions the gametophytes resumed growth or maturation within one month (Dieck, 1993). Intolerance to this factor is likely to be higher during the peak periods of sporulation and/or spore settlement.

    If inundation is long lasting then the understorey epifauna/flora may be adversely affected, e.g. suspension or filter feeding fauna and/or algal species.  This biotope occurs in high wave exposures and therefore deposited sediments are unlikely to remain for more than a few tidal cycles, except in the deepest of rock-pools. Therefore the effects of depositing 5 cm of fine sediment in a discrete event are likely to be transient.

    Sensitivity assessment. Resistance to the pressure is considered ‘High’, and resilience ‘High’. The sensitivity of this biotope to light deposition of up to 5 cm of fine material added to the seabed in a single discreet event is assessed as ‘Not sensitive’.

    High
    Low
    NR
    NR
    Help
    High
    High
    High
    High
    Help
    Not sensitive
    Low
    Low
    Low
    Help
    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

    Smothering by sediment e.g. 30 cm material during a discrete event, is unlikely to damage Laminaria hyperborea plants but is likely to affect gametophyte survival, holdfast communities, epiphytic community at the base of the stype, and interfere with zoospore settlement. Given the microscopic size of the gametophyte, 30 cm of sediment could be expected to significantly inhibit growth. However, laboratory studies showed that gametophytes can survive in darkness for between 6 - 16 months at 8 °C and would probably survive smothering within a discrete event. Once returned to normal conditions the gametophytes resumed growth or maturation within one month (Dieck, 1993). Intolerance to this factor is likely to be higher during the peak periods of sporulation and/or spore settlement.

    If clearance of deposited sediment occurs rapidly then understorey communities are expected to recover quickly. If inundation is long lasting then the understorey epifauna/flora may be adversely affected, e.g. suspension or filter feeding fauna and/or algal species.  While this  biotope occurs in high to moderate energy habitats (due to water flow or wave action) deposition of 30cm of sediment represents a large volume of material that would likely remain for a number of tidal cycles and is expected to damage understorey flora/fauna as well as juvenile Laminaria hyperborea.

    Sensitivity assessment. Resistance to the pressure is considered ‘Medium’, and resilience ‘High’. The sensitivity of this biotope to heavy deposition of up to 30cm of fine material added to the seabed in a single discreet event is assessed as ‘Low’.

    Medium
    Low
    NR
    NR
    Help
    High
    Low
    NR
    NR
    Help
    Low
    Low
    Low
    Low
    Help
    Litter [Show more]

    Litter

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

    Evidence

    Not assessed.

    Not Assessed (NA)
    NR
    NR
    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

    Not relevant (NR)
    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

    Shading of the biotope (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 'Medium' resilience and a sensitivity of 'Medium', albeit with 'low' confidence due to the lack of direct evidence.

    Low
    Low
    NR
    NR
    Help
    Medium
    Low
    NR
    NR
    Help
    Medium
    Low
    Low
    Low
    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.  But spore 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

    At the time of writing no evidence regarding the genetic modification or effects of translocation of native kelp populations was found.

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

    Sargassum muticum was shown to replace and out-compete leathery, canopy-forming macroalgae such as Saccharina latissima, Halidrys siliquosa, and Fucus spp. and, to a lesser degree, understorey species such as Codium fragile, Chondrus crispus and Dictyota dichotoma in Limfjorden, Denmark between 1984 and 1997 (Staehr et al., 2000; Engelen et al., 2015; de Bettignies et al., 2021). The invasion in Limfjorden had stabilized by 2005 although many of the native macroalgal species continued to decline (Engelen et al., 2015). In Limfjorden, the distribution of Sargassum muticum was limited to areas with hard substratum, in particular stones >10 cm in diameter, while smaller stones, gravel and sand were unsuitable. It was most abundant between 1 and 4 m in depth but had low cover at 0 to 0.5 m and 4 to 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). Viejo et al. (1995) reported that Sargassum muticum transplanted to wave exposed shores in Spain experienced >80% breakages within a month and that the growth of undamaged plants was significantly lower than that of plants on sheltered shores. Similarly, Andrew & Viejo (1998) noted that Sargassum muticum was restricted to intertidal rockpools in wave exposed sites in the Bay of Biscay.  

    Strong & Dring (2011) used canopy removal experiments to investigate inter- and intra-species competition between Sargassum muticum and Saccharina latissima in the Dorn, Strangford Lough, N. Ireland. The Dorn consists of tidal pools, very sheltered from wave action but with moderately strong tidal streams (1 - 2 knots). Sargassum muticum grew better in mixed stands with Saccharina latissima than in the highest-density monospecific stands examined. However, the growth of Saccharina was not affected by the proportion of Sargassum in mixed stands. They concluded that Saccharina was not impacted significantly by the alien species while Sargassum benefited from growth in mixed stands. Experimental manipulation of subtidal algal canopies in the San Juan Islands, Washington State, USA, showed that Sargassum muticum reduced the abundance of native macroalgae, including the kelp Laminaria bongardiana due to shading. However, the experimental removal of Sargassum resulted in the recovery of native species within about one year (Britton-Simmons, 2004; Engelen et al., 2015). The negative effects of Sargassum muticum on native macroalgae are mainly due to competition for light, rather than changes in nutrient availability, sedimentation or water flow (Britton-Simmons, 2004; Engelen et al., 2015).     

    Undaria pinnatifida (Wakame or Asian kelp) is a large brown seaweed and an Invasive Non-Indigenous Species (INIS) that could out-compete native UK kelp species (see Farrell & Fletcher, 2006; Thompson & Schiel, 2012; Brodie et al., 2014; Hieser et al., 2014; Arnold et al., 2016; Epstein & Smale, 2017; Epstein & Smale, 2018; Kraan, 2017; Epstein et al., 2019a,b; Tidbury, 2020). Undaria pinnatifida originates from Japan but is established currently on the coastlines of New Zealand, Australia, Northern France, Spain, Italy, the UK, Portugal, Belgium, Holland, Argentina, Mexico, and the USA (De Leij et al., 2017). Undaria pinnatifida was first recorded in the UK in the Hamble Estuary in 1994 (Macleod et al., 2016) and has since proliferated along UK coastlines. One year after its discovery at the Queen Anne Battery marina, Plymouth, it became a major fouling plant on pontoons (Minchin & Nunn, 2014). Although initially restricted to artificial habitats, such as marinas and ports, it is now widespread in natural habitats in several areas, including Plymouth Sound.  

    Undaria pinnatifida seems to settle better on artificial substrata (e.g., floats, marinas or piers) than on natural rocky shores among local kelps (Vaz-Pinto et al., 2014). It is found predominantly in low intertidal to shallow subtidal habitats (Epstein et al., 2019b) and is significantly more abundant on artificial substrata compared to natural rocky substrata (Heiser et al., 2014; Epstein & Smale, 2018). James (2017) suggested that Undaria pinnatifida could out-compete native species on artificial substrata (such as marinas and wharf structures). In Plymouth, UK, De Leij et al. (2017) found that natural habitats with dense native macroalgal canopies, such as Laminaria hyperborea, Laminaria ochroleuca, Laminaria digitata and Saccharina latissima had more resistance to Undaria pinnatifida invasion than disturbed or sparse canopies, due to limited space and light availability for Undaria pinnatifida recruits. However, the dense canopies did not always prevent the invasion of Undaria pinnatifida as sporophytes were still recorded within dense Laminaria canopies, so that canopy disturbance was not always required (De Leij et al., 2017; Epstein & Smale, 2018).  

    Undaria behaves as a winter annual, and recruitment occurs in winter followed by rapid growth through spring, maturity and then senescence through summer, with only the microscopic life stages persisting through autumn. It exhibits multiple dispersal strategies, such as short-range spore dispersal, and long-range dispersal as whole drift plants or fragments. Undaria pinnatifida has spread rapidly across the UK and Europe, resulting in community-wide responses and impacts (Vaz-Pinto et al., 2014; Epstein & Smale, 2017). Its impacts are complex and context-specific, depending on space, time, and taxa present in the introduced location (Epstein & Smale, 2017; Teagle et al., 2017; Tidbury, 2020).  

    Undaria pinnatifida has a wide physiological niche meaning it can occur in both coastal and estuarine environments showing tolerance for varying salinities, turbidity and siltation (Heiser et al., 2014; Epstein & Smale, 2018). Undaria pinnatifida has a greater preference for sites sheltered with low wave exposure and weak tidal streams (Heiser et al., 2014; Epstein & Smale, 2018). In natural habitats, Undaria pinnatifida was not recorded if the wave fetch was greater than 642 km but increased in abundance and cover in very sheltered sites (Epstein & Smale, 2018).  

    In St Malo, France, there was evidence that Undaria pinnatifida co-existed with Laminaria hyperborea under certain conditions (Castric-Fey et al., 1993). Epstein & Smale (2018) also observed that Undaria pinnatifida was relatively common (abundance of >70 individuals per 25 m transect) at three sites in Devon, UK (Jennycliff, Bovisand and Beacon Cove) where Laminaria spp. were abundant (40 - 79%) or superabundant (>80%), which suggested that Undaria pinnatifida could co-exist within refugia amongst areas with dense Laminaria spp.. 

    In Plymouth Sound, UK, Heiser et al. (2014) observed that Laminaria hyperborea was significantly less abundant at sites with the presence of Undaria pinnatifida, with only ca 0.5 Laminaria hyperborea individuals per m2 present compared to ca 8 individuals per m2 at sites without the presence of Undaria pinnatifida. However, the results from their correlation study only showed that the species were not found together (pers. comm., Epstein 2021). Whereas exclusion and succession experiments on reefs tell us that Laminaria spp. exclude Undaria pinnatifida, not the other way around. Epstein & Smale (2018) reported that in Devon, UK, persistent, dense, and intact Laminaria spp. canopies in rocky reef habitats exerted a strong influence over the presence/absence, abundance, and percentage cover of Undaria pinnatifida. A dense canopy of native kelp restricts the proliferation of Undaria pinnatifida and disturbance of the canopy is often the key to the recruitment of Undaria pinnatifida. Epstein et al. (2019b) reported that Undaria pinnatifida density and biomass were significantly negatively correlated with the sum of all Laminaria spp. in Plymouth, UK. The evidence indicated that native Laminaria spp. canopies in the UK inhibited Undaria pinnatifida and implied that Undaria pinnatifida was opportunistic but competitively inferior (Farrell & Fletcher, 2006; Heiser et al., 2014; Minchin & Nunn, 2014; De Leij et al., 2017; Epstein & Smale, 2018; Epstein et al., 2019b). However, Epstein et al. (2019b) also noted that Laminaria hyperborea had a non-significant positive relationship with Undaria pinnatifida due to low densities of Laminaria hyperborea across the study area, resulting in insufficient data. 

    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. De Leij et al. (2017) found that natural habitats with dense native macroalgal canopies, such as Laminaria hyperborea had more resistance to Undaria pinnatifida invasion than disturbed or sparse canopies, due to limited space and light availability for Undaria recruits. However, the dense canopies will not prevent the invasion of Undaria, as sporophytes were still recorded within dense Laminaria canopies, and this suggests that canopy disturbance is not always required. 

    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. The above evidence suggests that Undaria pinnatifida can co-exist with Laminaria hyperborea where sites are suitable e.g., Laminaria hyperborea in Plymouth Sound, UK. A dense kelp canopy may restrict or slow the proliferation of Undaria pinnatifida, however, there is mixed evidence of its colonization with Laminaria hyperborea beds and in some areas, a lower abundance of Laminaria hyperborea may result in increased Undaria pinnatifida growth. 

    This Laminaria hyperborea dominated biotope (IR.HIR.KFaR.LhypFa) is found within the upper infralittoral zone with extreme wave exposure and moderately strong to very weak tidal streams. The evidence above suggests that Sargassum muticum prefers sheltered, shallow sites in the sublittoral fringe. 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 Laminaria hyperborea beds was found. Therefore, competition with Sargassum is probably site-specific and dependent on local conditions, so it is unlikely to survive even in the shallow depths due to the wave exposed conditions that characterize this biotope. 

    Similarly, Undaria pinnatifida prefers sheltered conditions that are within its depth range (+1 to –4 m) and a low tidal flow, so like Sargassum it is unlikely that even in the shallow depths Undaria will out-compete or replace Laminaria hyperborea in this biotope due high degree of wave exposure. Therefore, resistance to Undaria or Sargassum is assessed as ‘High’, resilience as ‘High’, so sensitivity is ‘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

    Galls on the blade of Laminaria hyperborea and spot disease are associated with the endophyte Streblonema sp. although the causal agent is unknown (bacteria, virus or endophyte). Resultant damage to the blade and stipe may increase losses in storms. The endophyte inhibits spore production and therefore recruitment and recoverability (Lein et al., 1991).

    Sensitivity assessment. Resistance to the pressure is considered ‘Medium’, and resilience ‘High’. The sensitivity of this biotope to introduction of microbial pathogens is assessed as ‘Low’.

    Medium
    Low
    NR
    NR
    Help
    High
    High
    Low
    High
    Help
    Low
    Low
    NR
    NR
    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

    Christie et al. (1998) observed Laminaria hyperborea habitat regeneration following commercial Laminaria hyperborea trawling in south Norway. Within the study area trawling removed all large canopy-forming adult Laminaria hyperborea, however sub-canopy recruits were unaffected. Within 2-3 years of harvesting a new canopy had formed 1 m off the seabed. The associated holdfast communities recovered in 6 years however the epiphytic stipe community did not fully recover within the same time period. Christie et al., (1998) suggested that kelp habitats were relatively resistant to direct disturbance of Laminaria hyperborea canopy.

    Recurrent disturbance occurring at a smaller time scale than the recovery period of 2-6 years (stated above) could extend recovery time. Kain (1975) cleared sublittoral blocks of Laminaria hyperborea at different times of the year for several years. The first colonizers and succession community differed between blocks and at what time of year the blocks were cleared however within 2 years of clearance the blocks were dominated by Laminaria hyperborea. Leinaas & Christie (1996) also observed Laminaria hyperborea re-colonization of “urchin barrens”, following removal of urchins. The substratum was initially colinized by filamentous macroalgae and Saccharina latissima however after 2-4 years Laminaria hyperborea dominated the community.

    Following disturbance or in areas were recurrent rapid disturbance occurs Laminaria hyperborea recruitment could also be affected by interspecifc competitive interactions with Invasive Non Indigenous Species or ephemeral algal species (Brodie et al., 2014; Smale et al., 2013), however evidence for this is limited and thus not included within this assessment.

    Sensitivity assessment. Resistance to the pressure is considered ‘None’, and resilience ‘Medium’. The sensitivity of this biotope to damage to seabed surface features is assessed 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 Laminaria hyperborea from extraction of other marine resources, e.g. fisheries or aggregates, is likely to cause similar effects to that of direct harvesting of Laminaria hyperborea; hence the same evidence has been used for both pressure assessments.

    Christie et al. (1998) observed Laminaria hyperborea habitat regeneration following commercial Laminaria hyperborea trawling in south Norway. Within the study area trawling removed all large canopy-forming adult Laminaria hyperborea, however sub-canopy recruits were unaffected. Within 2-6years of harvesting a new canopy had formed 1m off the seabed. The associated holdfast communities recovered in 6 years however the epiphytic stipe community did not fully recover within the same time period. Christie et al., (1998) suggested that kelp habitats were relatively resistant to direct disturbance of Laminaria hyperborea canopy.

    Recurrent disturbance occurring at a smaller time scale than the recovery period of 2-6 years (stated above) could extend recovery time. Kain (1975) cleared sublittoral blocks of Laminaria hyperborea at different times of the year for several years. The first colonizers and succession community differed between blocks and at what time of year the blocks were cleared however within 2 years of clearance the blocks were dominated by Laminaria hyperborea. Leinaas & Christie (1996) also observed Laminaria hyperborea re-colonization of “urchin barrens”, following removal of urchins. The substratum was initially colinized by filamentous macroalgae and Saccharina latissima however after 2-4 years Laminaria hyperborea dominated the community.

    Following disturbance or in areas were recurrent rapid disturbance occurs Laminaria hyperborea recruitment could also be affected by interspecifc competitive interactions with Invasive Non Indigenous Species or ephemeral algal species (Brodie et al., 2014; Smale et al., 2013), however evidence for this is limited and thus not included within this assessment.

    Sensitivity assessment. Resistance to the pressure is considered ‘Low’, and resilience ‘Medium’. The sensitivity of this biotope to damage to seabed surface features is assessed as ‘Medium’.

    Low
    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. Arafeh-Dalmau, N., Montaño-Moctezuma, G., Martínez, J.A., Beas-Luna, R., Schoeman, D.S. & Torres-Moye, G., 2019. Extreme Marine Heatwaves Alter Kelp Forest Community Near Its Equatorward Distribution Limit. Frontiers in Marine Science, 6 (499). DOI https://doi.org/10.3389/fmars.2019.00499

    3. 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

    4. Assis, J., Araújo, M.B. & Serrão, E.A., 2018. Projected climate changes threaten ancient refugia of kelp forests in the North Atlantic. Global Change Biology, 24 (1), e55-e66. DOI https://doi.org/10.1111/gcb.13818

    5. Assis, J., Lucas, A.V., Bárbara, I. & Serrão, E.Á., 2016. Future climate change is predicted to shift long-term persistence zones in the cold-temperate kelp Laminaria hyperborea. Marine Environmental Research, 113, 174-182. DOI https://doi.org/10.1016/j.marenvres.2015.11.005

    6. Assis, J., Serrão, E.A., Claro, B., Perrin, C. & Pearson, G.A., 2014. Climate-driven range shifts explain the distribution of extant gene pools and predict future loss of unique lineages in a marine brown alga. Molecular Ecology, 23 (11), 2797-2810. DOI https://doi.org/10.1111/mec.12772

    7. Bekkby, T., Rinde, E., Erikstad, L. & Bakkestuen, V., 2009. Spatial predictive distribution modelling of the kelp species Laminaria hyperborea. ICES Journal of Marine Science, 66 (10), 2106-2115. DOI https://doi.org/10.1093/icesjms/fsp195

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

    9. 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

    10. Bishop, G.M., 1985. Aspects of the reproductive ecology of the sea urchin Echinus esculentus L. Ph.D. thesis, University of Exeter, UK.

    11. Bolton, J.J. & Lüning, K.A.F., 1982. Optimal growth and maximal survival temperatures of Atlantic Laminaria species (Phaeophyta) in culture. Marine Biology, 66, 89-94.

    12. Boney, A.D., 1971. Sub-lethal effects of mercury on marine algae. Marine Pollution Bulletin, 2, 69-71.

    13. 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

    14. Breeman, A.M., 1990. Expected Effects of Changing Seawater Temperatures on the Geographic Distribution of Seaweed Species. In Beukema, J.J., et al. (eds.). Expected Effects of Climatic Change on Marine Coastal Ecosystems, Dordrecht: Springer Netherlands, pp. 69-76. DOI: https://doi.org/10.1007/978-94-009-2003-3_9

    15. Britton, D., Cornwall, C.E., Revill, A.T., Hurd, C.L. & Johnson, C.R., 2016. Ocean acidification reverses the positive effects of seawater pH fluctuations on growth and photosynthesis of the habitat-forming kelp, Ecklonia radiata. Scientific reports, 6 (1), 26036. DOI: https://doi.org/10.1038/srep26036

    16. 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

    17. 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

    18. 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.

    19. 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.

    20. 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.

    21. 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

    22. Cazenave, A. & Nerem, R.S., 2004. Present-day sea-level change: Observations and causes. Reviews of Geophysics, 42 (3). DOI https://doi.org/10.1029/2003rg000139

    23. 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.

    24. Church, J.A. & White, N.J., 2006. A 20th century acceleration in global sea-level rise. Geophysical Research Letters, 33 (1). DOI https://doi.org/10.1029/2005gl024826

    25. Church, J.A., White, N.J., Coleman, R., Lambeck, K. & Mitrovica, J.X., 2004. Estimates of the Regional Distribution of Sea Level Rise over the 1950–2000 Period. Journal of Climate, 17 (13), 2609-2625.

    26. 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

    27. 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.

    28. Crisp, D.J. (ed.), 1964. The effects of the severe winter of 1962-63 on marine life in Britain. Journal of Animal Ecology, 33, 165-210.

    29. 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.

    30. 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.

    31. 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.

    32. 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

    33. 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

    34. 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.

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

    36. 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.

    37. Dinnel, P.A., Pagano, G.G., & Oshido, P.S., 1988. A sea urchin test system for marine environmental monitoring. In Echinoderm Biology. Proceedings of the Sixth International Echinoderm Conference, Victoria, 23-28 August 1987, (R.D. Burke, P.V. Mladenov, P. Lambert, Parsley, R.L. ed.), pp 611-619. Rotterdam: A.A. Balkema.

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

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

    40. 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.

    41. 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

    42. 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

    43. 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

    44. 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

    45. 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.

    46. 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.

    47. Fernández, P.A., Roleda, M.Y. & Hurd, C.L., 2015. Effects of ocean acidification on the photosynthetic performance, carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera. 124 (3), 293-304. DOI https://doi.org/10.1007/s11120-015-0138-5

    48. 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.

    49. 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].

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

    51. 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.

    52. Frölicher, T.L., Fischer, E.M. & Gruber, N., 2018. Marine heatwaves under global warming. Nature, 560 (7718), 360-364. DOI https://doi.org/10.1038/s41586-018-0383-9

    53. 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.

    54. 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.

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

    56. 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.

    57. 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.

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

    59. 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.

    60. 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)].

    61. Hoare, R. & Hiscock, K., 1974. An ecological survey of the rocky coast adjacent to the effluent of a bromine extraction plant. Estuarine and Coastal Marine Science, 2 (4), 329-348.

    62. 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.

    63. 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.

    64. Huthnance, J., 2010. Temperature and salinity, in: Charting the Progress 2: Ocean processes feeder report, section 3.2. (eds. Buckley, P., et al.): UKMMAS, Defra, London.

    65. Iñiguez, C., Carmona, R., Lorenzo, M.R., Niell, F.X., Wiencke, C. & Gordillo, F.J.L., 2016. Increased temperature, rather than elevated CO2, modulates the carbon assimilation of the Arctic kelps Saccharina latissima and Laminaria solidungula. 163 (12), 248. DOI https://doi.org/10.1007/s00227-016-3024-6

    66. Iñiguez, C., Carmona, R., Lorenzo, M.R., Niell, F.X., Wiencke, C. & Gordillo, F.J.L., 2016a. Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta. Polar Biology, 39 (11), 1979-1991. DOI https://doi.org/10.1007/s00300-015-1724-x

    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. Johansson ,G., Eriksson, B.K., Pedersen, M. & Snoeijs, P., 1998. Long term changes of macroalgal vegetation in the Skagerrak area. Hydrobiologia, 385, 121-138.

    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. Kinne, O. (ed.), 1984. Marine Ecology: A Comprehensive, Integrated Treatise on Life in Oceans and Coastal Waters.Vol. V. Ocean Management Part 3: Pollution and Protection of the Seas - Radioactive Materials, Heavy Metals and Oil. Chichester: John Wiley & Sons.

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

    86. 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

    87. Koch, M., Bowes, G., Ross, C. & Zhang, X.-H., 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology, 19 (1), 103-132. DOI https://doi.org/10.1111/j.1365-2486.2012.02791.x

    88. 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

    89. Krause-Jensen, D., Duarte, C.M., Hendriks, I.E., Meire, L., Blicher, M.E., Marbà, N. & Sejr, M.K., 2015. Macroalgae contribute to nested mosaics of pH variability in a subarctic fjord. Biogeosciences, 12 (16), 4895-4911. DOI https://doi.org/10.5194/bg-12-4895-2015

    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. Li, Y., Zhang, H., Tang, C., Zou, T. & Jiang, D., 2016. Influence of Rising Sea Level on Tidal Dynamics in the Bohai Sea. 74 (SI), 22-31. DOI https://doi.org/10.2112/si74-003.1

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

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

    98. 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

    99. 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.

    100. 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.

    101. 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

    102. 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.

    103. 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.

    104. 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.

    105. 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.

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

    107. Nepper-Davidsen, J., Andersen, D.T. & Pedersen, M.F., 2019. Exposure to simulated heatwave scenarios causes long-term reductions in performance in Saccharina latissima. Marine Ecology Progress Series, 630, 25-39
    108. Nichols, D., 1981. The Cornish Sea-urchin Fishery. Cornish Studies, 9, 5-18.

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

    110. 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.

    111. 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.

    112. 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.

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

    114. 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.

    115. Nunes, J., McCoy, S.J., Findlay, H.S., Hopkins, F.E., Kitidis, V., Queirós, A.M., Rayner, L. & Widdicombe, S., 2015. Two intertidal, non-calcifying macroalgae (Palmaria palmata and Saccharina latissima) show complex and variable responses to short-term CO2 acidification. ICES Journal of Marine Science, 73 (3), 887-896. DOI https://doi.org/10.1093/icesjms/fsv081

    116. O'Brien, P.J. & Dixon, P.S., 1976. Effects of oils and oil components on algae: a review. British Phycological Journal, 11, 115-142.

    117. Olischläger, M., Bartsch, I., Gutow, L. & Wiencke, C., 2012. Effects of ocean acidification on different life-cycle stages of the kelp Laminaria hyperborea (Phaeophyceae). Botanica Marina, vol. 55 pp. 511
    118. 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.

    119. 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.

    120. 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

    121. Pessarrodona, A., Moore, P.J., Sayer, M.D.J. & Smale, D.A., 2018. Carbon assimilation and transfer through kelp forests in the NE Atlantic is diminished under a warmer ocean climate. Global Change Biology, 24 (9), 4386-4398. DOI https://doi.org/10.1111/gcb.14303

    122. 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.

    123. Pickering, M.D., Wells, N.C., Horsburgh, K.J. & Green, J.A.M., 2012. The impact of future sea-level rise on the European Shelf tides. Continental Shelf Research, 35, 1-15. DOI https://doi.org/10.1016/j.csr.2011.11.011

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

    125. Rietema, H., 1993. Ecotypic differences between Baltic and North Sea populations of Delesseria sanguinea and Membranoptera alata. Botanica Marina, 36, 15-21.

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

    127. Rogers-Bennett, L. & Catton, C.A., 2019. Marine heatwave and multiple stressors tip bull kelp forest to sea urchin barrens. Scientific Reports, 9 (1), 15050. DOI https://doi.org/10.1038/s41598-019-51114-y

    128. Roleda, M.Y., Morris, J.N., McGraw, C.M. & Hurd, C.L., 2012. Ocean acidification and seaweed reproduction: increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Global Change Biology, 18 (3), 854-864. DOI https://doi.org/10.1111/j.1365-2486.2011.02594.x

    129. 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.

    130. 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.

    131. Schoenrock, K.M., O’Callaghan, T., O’Callaghan, R. & Krueger-Hadfield, S.A., 2019. First record of Laminaria ochroleuca Bachelot de la Pylaie in Ireland in Béal an Mhuirthead, county Mayo. Marine Biodiversity Records, 12 (1), 9. DOI https://doi.org/10.1186/s41200-019-0168-3

    132. Sheppard, C.R.C. & Bellamy, D.J., 1974. Pollution of the Mediterranean around Naples. Marine Pollution Bulletin, 5, 42-44.

    133. 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.

    134. 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.

    135. 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.

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

    137. Smale, D.A. & Vance, T., 2015. Climate-driven shifts in species’ distributions may exacerbate the impacts of storm disturbances on North-east Atlantic kelp forests. Marine and Freshwater Research, 67 (1), 65-74. DOI https://doi.org/10.1071/MF14155

    138. Smale, D.A., 2020. Impacts of ocean warming on kelp forest ecosystems. New Phytologist, 225, 1447-1454. DOI https://doi.org/10.1111/nph.16107

    139. 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.

    140. Smale, D.A., Epstein, G., Hughes, E., Mogg, A.O.M. & Moore, P.J., 2020. Patterns and drivers of understory macroalgal assemblage structure within subtidal kelp forests. Biodiversity and Conservation, 29 (14), 4173-4192. DOI https://doi.org/10.1007/s10531-020-02070-x

    141. Smale, D.A., Pessarrodona, A., King, N., Burrows, M.T., Yunnie, A., Vance, T. & Moore, P., 2020b. Environmental factors influencing primary productivity of the forest-forming kelp Laminaria hyperborea in the northeast Atlantic. Scientific Reports, 10 (1), 12161. DOI https://doi.org/10.1038/s41598-020-69238-x

    142. Smale, D.A., Wernberg, T., Oliver, E.C.J., Thomsen, M., Harvey, B.P., Straub, S.C., Burrows, M.T., Alexander, L.V., Benthuysen, J.A., Donat, M.G., Feng, M., Hobday, A.J., Holbrook, N.J., Perkins-Kirkpatrick, S.E., Scannell, H.A., Sen Gupta, A., Payne, B.L. & Moore, P.J., 2019. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nature Climate Change, 9 (4), 306-312. DOI https://doi.org/10.1038/s41558-019-0412-1

    143. 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.

    144. Smale, D.A., Wernberg, T., Yunnie, A.L.E. & Vance, T., 2015. The rise of Laminaria ochroleuca in the Western English Channel (UK) and comparisons with its competitor and assemblage dominant Laminaria hyperborea. Marine Ecology, 36 (4), 1033-1044. DOI https://doi.org/10.1111/maec.12199

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

    146. 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.

    147. 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

    148. Steinhoff, F.S., Wiencke, C., Müller, R. & Bischof, K., 2008. Effects of ultraviolet radiation and temperature on the ultrastructure of zoospores of the brown macroalga Laminaria hyperborea. 10 (3), 388-397. DOI https://doi.org/10.1111/j.1438-8677.2008.00049.x

    149. 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.

    150. 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.

    151. Stock, J.H., 1988. Lamippidae (Copepoda : Siphonostomatoida) parasitic in Alcyonium. Journal of the Marine Biological Association of the United Kingdom, 68 (2), 351-359.

    152. 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.

    153. 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

    154. 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.

    155. 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

    156. 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].

    157. 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.

    158. 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.

    159. 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.

    160. 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

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

    162. 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.

    163. Wilkinson, M., 1995. Information review on the impact of kelp harvesting. Scottish Natural Heritage Review, no. 34, 54 pp.

    164. 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., Hiscock, K., Garrard, S.L.,, Burdett, E.G. & Tyler-Walters, H., 2023. Laminaria hyperborea forest with a faunal cushion (sponges and polyclinids) and foliose red seaweeds on very exposed upper infralittoral rock. 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 29-03-2024]. Available from: https://www.marlin.ac.uk/habitat/detail/44

     Download PDF version


    Last Updated: 26/10/2023