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information on the biology of species and the ecology of habitats found around the coasts and seas of the British Isles

Sabellaria spinulosa with kelp and red seaweeds on sand-influenced infralittoral rock

17-09-2018

Summary

UK and Ireland classification

Description

Laminaria hyperborea kelp forest on shallow infralittoral bedrock and boulders characterized by encrustations of Sabellaria spinulosa tubes that cover much of the rock, together with sand-tolerant red seaweeds such as Phyllophora pseudoceranoides, Dilsea carnosa and Polysiphonia elongata and Polysiphonia fucoides. Red seaweeds such as Plocamium cartilagineum and Delesseria sanguinea may also be found beneath the kelp canopy, although typically low in abundance. They can be colonized by the ascidian Botryllus schlosseri. The cowrie Trivia arctica can also be found here. Much of the available rock is covered with encrusting coralline algae together with patches of the encrusting sponge Halichondria panicea and the sea anemone Urticina felina. More mobile fauna include the echinoderms Asterias rubens, Henricia sanguinolenta, Echinus esculentus and Ophiothrix fragilis, the gastropod Gibbula cineraria and the hermit crab Pagurus bernhardus. The scouring effect of mobile sand adjacent to the rock maintains a reduced underflora and fauna compared to the association of species found in non-scoured kelp forests (Lhyp.Ft). Scour-resistant fauna such as the barnacle Balanus crenatus can be locally abundant on the rock, while the bivalve Pododesmus patelliformis can be found seeking shelter underneath the cobbles. Above the effect of scour, kelp stipes may be densely colonized by red seaweeds such as Phycodrys rubens, Palmaria palmata and Membranoptera alata, together with some sponges and ascidians.  This biotope is found in the sand-laden waters of north-east England in conditions in which Sabellaria spinulosa  is able to thrive. Nearby circalittoral rock is often also dominated by Sabellaria spinulosa  (Sspi) but lacks the kelp and red seaweeds. This biotope is not commonly recorded in the UK so there is a lack of information relating to the surrounding biotopes. (Information from Connor et al., 2004; JNCC, 2015). 

Depth range

0-5 m, 5-10 m

Additional information

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Habitat review

Ecology

Ecological and functional relationships

  • Sabellaria spinulosa colonize scoured rock rapidly and may be sufficiently dense to prevent the settlement or attachment of other species to the substratum, although the crust itself may act as a substratum for other fauna and flora.
  • Sabellaria spinulosa requires suspended sand grains in order to form its tubes; reef communities therefore, only occur in turbid areas where sand is placed into suspension by water movement.
  • Kelps are major primary producers, up to 90% of kelp production enters the detrital food web and 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. Kelp holdfasts provide both substrata and refugia for a huge diversity of macroinvertebrates. Kelp beds are diverse species rich habitats and over 1,800 species have been recorded in the UK kelp biotopes (Birkett et al., 1998b).
  • Epiphytes and understorey algae are grazed by a variety of amphipods, isopods and gastropods, e.g. Littorina spp., Acmaea spp., Haliotis tuberculata, Aplysia and rissoid gastropods (Birkett et al., 1998b).
  • Sabellaria spinulosa and other associated organisms in the biotope, may be an important source of food for the pink shrimp Pandalas montagui. The biotope may also be an important feeding ground for fish.
  • Suspension feeders, such as Sabellaria spinulosa, Ophiothrix fragilis, sponges, bryozoans and ascidians are the dominant fauna in the biotope. The top shell Steromphala cineraria is the only common grazer in the biotope although Echinus esculentus is also sometimes present. The anemone Urticina felina is a passive carnivore, waiting to trap animals that stumble into its tentacles.
  • Although not present in large numbers in the biotope Echinus esculentus can have an influence in the biotope. The species graze the under-canopy and understorey algae, including juvenile kelp sporophytes, together with epiphytes and epifauna on the lower reaches of the laminarian stipe. Wave action and abrasion between stipes probably knocks urchins off the upper stipe. It is likely that urchins will graze the Sabellaria spinulosa. Sea urchin grazing may maintain the patchy and species rich understorey epiflora/fauna by preventing dominant species from becoming established.

Seasonal and longer term change

  • Sabellaria spinulosa is a fast growing annual species and crusts up to 2-3cm thick can develop within one growing season. High recruitment of Sabellaria spinulosa may result in 'reinforcement' of the crust of tubes on the substratum. Reproductive seasonality of Sabellaria spinulosa is unclear, but spawning probably occurs largely over winter and settlement in early spring (Holt et al., 1998).
  • 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 plants become liable to removal by wave action and storms due to their size and weakening by grazers such as Patella pellucida. Loss of older plants results in more light reaching the understorey, temporarily permitting growth of algae including Laminaria hyperborea sporelings.
  • Many species of red algae are perennial exhibiting strong seasonal patterns of growth and reproduction. Delesseria sanguinea, for example, produces new blades in February and grows to full size by May - June becoming increasing battered or torn and the lamina are reduced to midribs by December (Maggs & Hommersand 1993).
  • Several other species, including hydroids, are annuals and abundance may show seasonal changes.

Habitat structure and complexity

The crusts of Sabellaria spinulosa appear to have a considerable influence on community structure by providing a single species sheet that may be unstable for other species to attach to. The development of a diverse community may be dependent on space being made in the Sabellaria crust and other species settling on the rock. Diversity on crusts is not high. It might be that the richest communities occur where Sabellaria is not dominant. This is in contrast to Sabellaria spinulosa reefs on mobile substrata such as cobbles and pebbles which are stabilised by the crusts and often have a higher diversity and abundance of fauna than nearby areas (George & Warwick, 1985) with fauna such as sponges, ascidians, hydroids and bryozoans attached to the crust. The presence of kelp plants, and other algae, contribute to increases in structural complexity as the fronds, stipe and holdfast provide substratum and shelter for a great diversity and abundance of epiphytic algae and sessile fauna.

Productivity

Productivity in the biotope is a mixture of primary and secondary productivity. Kelps are the major primary producers in UK marine coastal waters producing nearly 75 % 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. However, kelp abundance, and hence productivity is not as high in the MIR.SabKR biotope as some other infralittoral biotopes (e.g. see EIR.LhypR). Many of the other species in the biotope, such as Sabellaria spinulosa and Ophiothrix fragilis, are suspension feeders feeding on detritus and phytoplankton.

Recruitment processes

Most species present in the MIR.SabKR biotope possess a planktonic stage (gamete, spore or larvae) which float in the plankton before settling and metamorphosing into the adult form. This provides the potential for dispersal over considerable distances allowing many of the species in the biotope to rapidly colonize new areas that become available such as in the gaps often created by storms. The recruitment processes of key characteristic or dominant species are described here.
  • Recruitment of Sabellaria spinulosa can be very variable. The larvae of Sabellaria spinulosa spend between six weeks and two months in the plankton (Wilson, 1970b) and so dispersal range is likely to be considerable. Larvae are strongly stimulated to settle by cement secretions of adult or newly settled individuals. In the absence of suitable stimulation metamorphosis and settlement occurs but always more slowly. High recruitment of Sabellaria spinulosa may result in 'reinforcement' of the crusts of tubes on the substratum.
  • Laminaria hyperborea produces vast numbers of spores, however they need to settle and form gametophytes within about 1 mm of each other 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. Most young sporophytes (germlings) appear in spring but can appear all year round depending on conditions (Birkett et al. 1998b).
  • Rhodophyceae have non flagellate, and non-motile spores that stick on contact with the substratum. Norton (1992) noted that algal spore dispersal is probably determined by currents and turbulent deposition. However, red algae produce large numbers of spores that may settle close to the adult especially where currents are reduced by an algal turf or in kelp forests.
  • Reproductive types of Lithophyllum incrustans occur from October to April but tail-off into summer. It has been calculated that 1 mm x 1mm of reproductive thallus produces 17.5 million bispores per year with average settlement of only 55 sporelings/year (Edyvean & Ford, 1984). However, spores will settle and new colonies will arise rapidly on bare substratum although growth rate is slow (2-7 mm per annum - see Irvine & Chamberlain, 1994).
  • Some characterizing species may not recruit so readily, for instance the larvae of Urticina felina inhabits the water column, but is not considered to be truly pelagic and probably has limited dispersal abilities (Solé-Cava et al., 1994).

Time for community to reach maturity

Sabellaria spinulosa seems in many cases to acts as a fast growing annual and early colonizer, but on more stable reefs the animals seem to be able to live for a few years. A typical lifespan for the littoral Sabellaria alveolata living in colonies forming reefs on bedrock in Duckpool was 4-5 years (Wilson, 1971). Areas where Sabellaria spinulosa had been lost due to winter storms appeared to recolonize quickly up to the maximum observed crust thickness (2.4 cm) during the following summer (R. Holt pers. comm. cited in Holt et al., 1998). Linke (1951) reported that spawning of intertidal Sabellaria spinulosa reefs in the southern North Sea took place during the first and second years. Thus, in ideal conditions, sexual maturity of Sabellaria spinulosa is probably reached within the first year. The algae in the biotope are also likely to reach maturity fairly rapidly. Experimental clearance experiments in the Isle of Man (Kain 1975a; Kain, 1979) showed that Laminaria hyperborea returned to near control levels of biomass within 3 years at 0.8 m and the species reaches sexual maturity at between two and six years of age. Sivertsen (1991 cited in Birkett et al., 1998b), showed that kelp populations stabilise about 4-5 years after harvesting. However, many of the other species, the anemone Urticina felina and coralline algae for example, within the reef matrix are slow growing and long-lived with a very low turnover rate. Lithophyllum incrustans in particular is very slow growing (2-7 mm per annum) and colonies may be up to 30 years old (Irvine & Chamberlain, 1994). Species diversity on the Sabellaria crust is likely to increase with age of the reef so although most components of the biotope can reach maturity within several years full community diversity and complexity is likely to take much longer.

Additional information

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Preferences & Distribution

Habitat preferences

Depth Range 0-5 m, 5-10 m
Water clarity preferencesNo information
Limiting Nutrients Nitrogen (nitrates), Phosphorus (phosphates)
Salinity preferences Full (30-40 psu)
Physiographic preferences Open coast
Biological zone preferences Infralittoral
Substratum/habitat preferences Bedrock, Large to very large boulders, Small boulders
Tidal strength preferences Very Weak (negligible), Weak < 1 knot (<0.5 m/sec.)
Wave exposure preferences Moderately exposed
Other preferences Sand-scoured

Additional Information

  • No specific information is available regarding temperature preferences of tolerances for this biotope. The distribution of the key structural species Sabellaria spinulosa and Laminaria hyperborea extend to the north and south of the British Isles and so will be exposed to higher and lower temperatures than experienced locally.
  • High levels of suspended sediment are likely to be required in order for Sabellaria spinulosa to construct its tubes.

Species composition

Species found especially in this biotope

    Rare or scarce species associated with this biotope

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    Additional information

    Sensitivity review

    Sensitivity characteristics of the habitat and relevant characteristic species

    This biotope IR.MIR.KR.Lhyp.Sab is characterized by Laminaria hyperborea kelp forest influenced by sand. The resultant scour reduces the abundance of red macroalgal and faunal turf understorey compared to typical kelp and rea seaweed biotopes (KR) e.g. IR.MIR.KR.Lhyp.Ft.  The suspended sediment also allows crusts of Sabellaria spinulosa to become abundant, further restricting substratum for foliose red seaweeds and faunal turf species, except for scour-resistant species such as Balanus crenatus, which may be locally abundant. However, the red algae, sponge and ascidian epiphytes typical of kelp stipes can occur above the level of surface scour.  This biotope (KR.Lhyp.Sab) may represent a transition habitat between the infralittoral kelp biotopes and the circalittoral sand scour dominated Sabellaria spinulosa (CR.MCR.CSab.Sspi).

    Loss of the kelp species would probably result in a faunal turf and Sabellaria crust dominated biotope, whereas loss of the scour and Sabellaria crusts would probably result in a typical Laminaria hyperborea dominated kelp forest biotope.  Therefore, sensitivity assessment is based on the sensitivity of the two characteristic structural species, Laminaria hyperborea and Sabellaria spinulosa.  The red algal flora and understorey would increase in abundance if the scour and Sabellaria crusts were lost, and the diversity of epiphytes is dependent on the presence of  Laminaria hyperborea stipes. However, their sensitivity is mentioned where relevant.  Other transient, opportunistic, or mobile species are probably ubiquitous and are not directly considered in the sensitivity assessment. 

    Resilience and recovery rates of habitat

    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, 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 ~200 m (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).

    Several 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 six years (Birkett et al., 1998b). Full epiphytic community and stipe habitat complexity regeneration require over six 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 (1975a) 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 the time of year the blocks were cleared, however within 2 years of clearance the blocks were dominated by Laminaria hyperborea.

    In south Norway, Laminaria hyperborea forests are harvested, which results in large scale removal of the canopy-forming kelps. Christie et al. (1998) found that in south Norwegian Laminaria hyperborea beds a pool of small (<25 cm) 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 one metre within 2-6 years after kelp harvesting. Within one year following harvesting, and each successive year thereafter, a pool of Laminaria hyperborea recruits had re-established within the understorey beneath the kelp canopy. Christie 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 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, 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 (Christie 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). Whereas these theories are largely unproven a number of studies have shown the removal of urchins from grazed areas coincide 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, whereas '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 on 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.

    Evidence to assess the likely recovery rate of Sabellaria spinulosa reefs from impacts is limited and significant information gaps regarding recovery rates, stability and persistence of Sabellaria spinulosa reefs exist (Gibb et al., 2014). The use of evidence from different population densities e.g. between thin crusts and thick reefs and between Sabellaria spinulosa and the congener Sabellaria alveolata must, therefore, be treated cautiously as the evidence may not be applicable.  Recovery of impacted populations will always be mediated by stochastic events and processes acting over different scales including, but not limited to, local habitat conditions, further impacts and processes such as larval-supply and recruitment between populations (Gibb et al., 2014). 

    The reproductive phase appears to be relatively long and Sabellaria spinulosa larvae spend 6-8 weeks in the plankton (Wilson, 1970b).  As a result, there is a good larval supply with high dispersal potential.  Pearce et al. (2011a) found that separating the adult Sabellaria spinulosa from tubes in the laboratory, induced gamete release. Pearce et al. (2011a) suggested this was a ‘significant evolutionary development whereby Sabellariid polychaetes spawn in response to disturbance as a means of potentially securing the future population’.  Several studies have indicated that the major spawning event is in the spring.  Plankton trawls revealed a high abundance of Sabellaria spinulosa larvae in February 2008 and smaller numbers in September and November 2009 (Pearce et al., 2011a).  Garwood (1982) found planktonic larvae on the north-east coast of England from August to November. These findings suggest that the main spawning event is at the beginning of the year but larvae are produced throughout the subsequent months. A February spawning event resulting in spring settlement is supported by the findings of George & Warwick (1985) and Wilson (1970a), who reported larval settlement in March in the Bristol Channel and Plymouth areas respectively. These findings suggest colonization of suitable habitats may be most likely in the spring but could occur over extended periods.

    However, successful recruitment may be episodic. Wilson (1971) cites the work of Linke (1951) who recorded the appearance of Sabellaria spinulosa reefs on stone-work of intertidal protective groynes.  In 1943 no colonies were present (time of year of this observation is unknown) but by September 1944 there were reefs 6-8 m wide and 40-60 cm high stretching for 60 m.  Linke (1951) assumed that the settlement took place in 1944.  In the summer of 1945 many colonies were dead and those remaining ceased growth in the autumn.  Thick reefs may, therefore, develop rapidly and decline quickly. It should be noted, that these results should be interpreted cautiously, due to the possibility that the observed species may have been Sabellaria alveolata (Bryony Pearce, pers comm.).

    The longevity of Sabellaria spinulosa reefs is not known and may vary between sites depending on local habitat conditions.  In naturally disturbed areas reefs may undergo annual cycles of erosion and recolonization (Holt et al., 1998).  Surveys on the North Yorkshire and Northumberland coasts found that areas where Sabellaria spinulosa had been lost due to winter storms, appeared to be recolonized up to the maximum observed 2.4 cm thickness during the following summer (R. Holt pers comm., cited from Holt et al., 1998).  Recovery of thin encrusting reefs may, therefore, be rapid. 

    Reefs may persist for long periods n some areas, although there is a significant lack of studies on the temporal stability of Sabellaria spinulosa reefs (Limpenny et al., 2010).  It has been suggested that the tubes of the worm can persist for some time in the marine environment. Therefore, the age of the colony may exceed the age of the oldest individuals present (Earll & Erwin, 1983).  Laboratory experiments have suggested that larvae settle preferentially on old tubes (Wilson, 1970b).  Therefore, providing environmental conditions are still favourable, the recovery of senescent or significantly degraded reefs through the larval settlement is stimulated by the presence of existing tubes (Earll & Erwin, 1983).

    Studies of reefs of the congener Sabellaria alveolata within the low intertidal suggest that areas of small, surficial damage within reefs may be rapidly repaired by the tube building activities of adult worms.  Vorberg (2000) found that trawl impressions made by a light trawl in Sabellaria alveolata reefs disappeared four to five days later due to the rapid rebuilding of tubes by the worms.  Similarly, studies of intertidal reefs of Sabellaria alveolata by Cunningham et al. (1984) found that minor damage to the worm tubes as a result of trampling, (i.e. treading, walking or stamping on the reef structures) was repaired within 23 days. However, more severe, localised damage caused by kicking and jumping on the reef structure, resulted in large cracks between the tubes, and removal of sections (ca 15x15x10 cm) of the structure (Cunningham et al., 1984).  Subsequent wave action enlarged the holes or cracks.  However, after 23 days, at one site, one side of the hole had begun to repair, and tubes had begun to extend into the eroded area.  At another site, a smaller section (10x10x10 cm) was lost but, after 23 days, the space was already smaller due to rapid growth (Cunningham et al., 1984).  Sabellaria spinulosa reefs are more fragile than Sabellaria alveolata (Bryony Pearce, pers comm, 2014, cited in Gibb et al., 2014) and recovery rates between reefs made by the two species may vary but this has not been established.

    Where reefs are extensively damaged or removed, then recovery will rely on larval recolonization.  Sabellaria spinulosa reproduction was studied by Wilson (1970a&b), Pearce et al. (2007) and Pearce et al. (2011b). Individuals may reach sexual maturity rapidly. Linke (1951) reported that Sabellaria spinulosa inhabiting the intertidal spawned at 1 or 2 years old and growth rate studies by Pearce et al. (2007) also suggested that sexual maturity in subtidal populations could be reached within the first year.  Pearce et al. (2007) constructed size-frequency histograms based on wet weight of complete Sabellaria spinulosa collected from the Hastings Shingle Bank, which suggested that Sabellaria spinulosa was capable of rapid growth, approaching maximum adult biomass within months (Pearce et al., 2007).

    Studies within and adjacent to the Hastings Shingle Bank aggregate extraction area demonstrate a similarly rapid recolonization process (Cooper et al., 2007; Pearce et al., 2007).  Recolonization within two previously dredged areas appeared to be rapid. Substantial numbers of Sabellaria spinulosa were recorded in one area in the summer after cessation of dredging activities and another area was recolonized within 16-18 months (Pearce et al., 2007).  Therefore, recruitment was annual rather than episodic in this area.  Recovery to the high abundance and biomass of more mature reefs was considered to require 3-5 years if larval recruitment was successful every year (Pearce et al., 2007).

    However, in some cases reefs may not recover once removed. The Wadden Sea has experienced a widespread decline of Sabellaria spinulosa over recent decades with little sign of recovery.  This is thought to be partly due to ecosystem changes (Reise et al., 1989; Buhs & Reise, 1997) exacerbated by fishing pressures that continue (Riesen & Reise, 1982; Reise & Schubert, 1987).  Likewise, no recovery of Sabellaria spinulosa has occurred in the approach channels to Morecambe Bay (Mistakidis 1956; cited from Holt et al., 1998).  This observation is believed this is due to a lack of larval supply or larval settlement, since larvae may preferentially settle on existing adult reefs (although directly settlement on sediments also occurs), or alterations in habitat (Holt et al., 1998).

    Resilience assessment. The evidence for recovery rates of Sabellaria spinulosa reefs from different levels of impact is very limited and the rates at which reefs recover from different levels of impact, and any similarity in rates or not between biotopes, have not been documented.  Recovery rates are likely to be determined by a range of factors such as the degree of impact, the season of impact, larval supply and local environmental factors including hydrodynamics.  The evidence from Sabellaria alveolata reefs (Vorberg, 2000; Cunningham et al., 1984) suggests that areas of limited damage on a reef, e.g. where resistance is 'Medium', could be repaired rapidly (within weeks) through the tube-building activities of adults.  It is not known if Sabellaria spinulosa exhibits the same response but resilience is assessed as ‘High’ in this instance. Predicting the rate of recovery following extensive removal is more problematic. Some thin crusts of Sabellaria spinulosa are relatively ephemeral and disappear following natural disturbance such as storms but recover the following year (Holt et al., 1998), suggesting that recovery is ‘High’ (within 2 years), even where reefs are removed. In other instances, recolonization has been observed within 16-18 months.  However, Pearce et al. (2007) suggested that full recovery to a state similar to the pre-impact condition of high adult density and adult biomass required three to five years where recruitment is annual.  Therefore, recovery from significant impacts (where resistance is assessed as ‘None’ or 'Low') is probably ‘Medium’ (2-10 years).

    The evidence suggests that beds of mature Laminaria hyperborea can regenerate from disturbance within 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. 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.  Therefore, resilience is probably  'Medium' (2-10 years).

    In summary, the crusts of Sabellaria spinulosa that characterize this biotope may exhibit natural cycles of erosion and growth (e.g. after storms) and recover in the following year so that where the pressure under assessment results in 'some' damage to the crusts alone (a resistance of 'Medium') resilience is probably 'High'. However, where pressures result in 'some' damage to the kelp forest component of the biotope (a resistance of 'Medium') then resilience is probably 'Medium'. Nevertheless, where pressures result in 'significant' or 'severe' damage to the biotope (a resistance of 'Low' and 'None' respectively) then resilience is assessed as 'Medium' (2-10 years). The affected components of the biotope are highlighted where required. There is good evidence on the recovery of kelp dominated habitats but limited evidence on the recovery of Sabellaria crusts from impacts. Therefore, the confidence in the quality of the evidence varies between different components of the biotope. Therefore, confidence in the quality of the evidence is assessed as ‘Medium’; the applicability of the evidence is also assessed as ‘Medium’ while the concordance is assessed as ‘Medium’ based on an agreement in direction but not magnitude, that is, the rate of recovery between studies.

    Please note as in Northern Norway urchin grazing pressure could extend the recovery 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) suggest could be a more damaging than the individual pressures.

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

    Hydrological Pressures

    Use / to open/close text displayedResistanceResilienceSensitivity
    Medium Medium Medium
    Q: High
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium

    Kain (1964) reported that Laminaria hyperborea sporophyte growth and reproduction could occur within a temperature range of 0°C and 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., 1998b). 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 also vary seasonally and temperature changes are less tolerated in winter months than summer months (Birkett et al., 1998b). However, it has a wide distribution in the North East Atlantic from Iceland south to the Bay of Biscay and Portugal. 

    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).  A 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.

    No empirical evidence was found for the temperature tolerance of Sabellaria spinulosa.  Nevertheless, its widespread distribution suggests that it is tolerant of temperature variation (Gibb et al., 2014). Sabellaria spinulosa has the greatest geographical range of all the sabellariids, according to current records, encompassing Iceland, the Skagerrak and the Kattegat, the North Sea, the English Channel, the northeast Atlantic, the Mediterranean, the Wadden Sea and the Indian Ocean, (Achari, 1974; Riesen & Reise, 1982; Reise & Schubert,1987; Hayward & Ryland, 1998; Foster-Smith, 2000; Collins, 2005). The associated epifauna are highly variable and reflect the assemblages found in adjacent biotopes. 

    Sensitivity assessment. In the UK, northern to southern Sea Surface Temperature (SST) ranges from 8-16°C in summer and 6-13°C in winter (Beszczynska-Möller & Dye, 2013). Overall, a chronic change (2°C for a year) outside the 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, although Sabellaria crusts are probably resistant.  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 assessed as 'Medium' and resilience as  'Medium' so that the sensitivity of this biotope to increases in temperature is assessed as 'Medium'.

    High High Not sensitive
    Q: High
    A: High
    C: Medium
    Q: High
    A: High
    C: High
    Q: High
    A: High
    C: Medium

    Kain (1964) reported that Laminaria hyperborea sporophyte growth and reproduction could occur within a temperature range of 0°C and 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., 1998b). 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., 1998b), 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).  Also, the average annual sea temperature, from 1970 to 2014, was 8°C (Beszczynska-Möller & Dye, 2013). The available information suggests that Laminaria hyperborea forest and canopy would not be affected by a decrease in sea temperature at the benchmark level.

    Sabellaria spinulosa occurs north to the Arctic and is, therefore, probably tolerant of a decrease in temperature at the pressure benchmark. This conclusion is supported by observations that Sabellaria spinulosa appeared unaffected by the cold, on oyster grounds in the River Crouch, throughout the severe winter of 1962–1963 The mean daily temperature was recorded at a depth of one fathom (1.8 m) below low water (equinoctial spring tide) and the lowest temperature recorded was -1.8°C (Crisp, 1964). At Penmon in Bangor, Sabellaria spinulosa also did not to suffer from the low temperatures and live individuals were found readily (Crisp, 1964). 

    Sensitivity assessment. Therefore, the evidence suggests that neither the Laminaria hyperborea canopy nor the Sabellaria crusts would be adversely affected by a decrease in temperature at the benchmark level. Therefore, resistance to the pressure is assessed as ‘High’ and resilience as ‘High’ so that the sensitivity of this biotope to a decrease in temperature is assessed as ‘Not Sensitive’ at the benchmark level. 

    Medium Medium Medium
    Q: Low
    A: NR
    C: NR
    Q: Medium
    A: Medium
    C: Medium
    Q: Low
    A: Low
    C: Low

    Lüning (1990) suggested that 'kelps' were stenohaline and that their general tolerance to salinity as a phenotypic group covered 16-50 psu over a 24 hr period. Optimal growth probably occurs between 30-35 psu ('Full' salinity) and growth rates are likely to be affected by periodic salinity stress. Birkett et al. (1998b) 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. No evidence for the physiological tolerance of Sabellaria spinulosa to salinity change was found by Gibb et al. (2014).  Roberts et al. (2010b) reported that hypersaline effluents from desalination plants disperse with tens of metres of the discharge point but reported widespread alteration in seagrass and soft sediment communities in poorly flushed environments. Hypersaline effluents are likely to sink to the seabed, and potentially penetrate the sediment. However, the water movement characteristic of this biotope is likely to disperse the effluent and limit the effect to the immediate vicinity of any discharge point.

    Sensitivity assessment. The evidence suggests that the Laminaria hyperborea canopy might be affected by hypersaline conditions. Therefore, a precautionary resistance assessment of 'Medium' is suggested but with Low confidence. Resilience is probably 'Medium' so that sensitivity is assessed as 'Medium'.

    Low Medium Medium
    Q: High
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium

    Lüning (1990) suggested that 'kelps' were stenohaline and that their general tolerance to salinity as a phenotypic group covered 16-50 psu over a 24 hr period. Optimal growth probably occurs between 30-35 psu ('Full' salinity) and growth rates are likely to be affected by periodic salinity stress. Birkett et al. (1998b) 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, but that growth was reduced at 16 psu and sporophytes did not grow at 7 psu. A decrease in one MNCR salinity scale from 'Full' salinity (30-40 psu) to 'Reduced' salinity (18-30 psu) could result in a decrease of Laminaria hyperborea sporophyte growth. Laminaria hyperborea may also be out-competed by low salinity tolerant species e.g. Saccharina latissima (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 latissima 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., 1998b; Christie et al., 1998). The ability of Laminaria hyperborea to out-compete Undaria pinnatifida within the UK is, however, unknown (Heiser et al., 2014), and any interspecific interaction between Laminaria hyperborea and Undaria pinnatifida is not included within this sensitivity assessment.

    No evidence for the physiological tolerances of Sabellaria spinulosa to decreases in salinity was found by Gibb et al. (2014).  Sabellaria spinulosa does not seem to occur in very low salinity areas (Holt et al.,1998) but has been recorded from estuaries including the Crouch, Mersey (Killeen & Light, 2000) and the Thames (Limpenny, 2010).  Buhs & Reise (1997) surveyed 12 channel systems in the Wadden Sea and found that Sabellaria spinulosa reefs occurred in the northern tidal inlets that experienced salinity levels ranging from 28 to 30 psu.  There is some speculation (Foster-Smith & Hendrick, 2003) that Mcintosh (1922) misidentified samples of Sabellaria spinulosa as the congener Sabellaria alveolata from the Humber estuarine population (Holt et al., 1998).  These records indicate that reduced and variable salinities can be tolerated to some extent but the paucity of records suggests that areas of reduced salinity do not provide optimal habitat. 

    Sensitivity assessment. Therefore a reduction in salinity from 'Full' (30-35) to 'Reduced' (18-30) for a year, may result in loss of a proportion of the kelp bed, as sporophyte growth is reduced and loss by wave action and herbivory increases, or via competion with opportunistic, low salinity tolerant, species such as Saccharina latissima. Similarly, Sabellaria may not be able to tolerate low salinities, although the evidence is unclear. Therefore, resistance to the pressure is assessed as ‘Low’, and resilience ‘Medium’ so that the sensitivity of this biotope to decreases in salinity is assessed as ‘Medium’.

    High High Not sensitive
    Q: High
    A: High
    C: Medium
    Q: High
    A: High
    C: High
    Q: High
    A: High
    C: Medium

    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 to April 2010. Maximal significant wave height (Hm0) was 3.67 & 2 m and maximal water velocity (Velrms) was 0.6 & 0.3 m/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 varies 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). Increased 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).

    Sabellaria spinulosa tends to occur in areas of high water movement where larvae, tube building materials and food particles are suspended and transported (Jones et al., 2000).  The relative importance of tidal versus wave induced movements to support reefs is, however, unclear (Holt et al., 1998). There is limited in-situ data on the specific water flow tolerances of Sabellaria spinulosa, although colonies have been found in areas with sedimentary bed forms that suggest current velocities in the range of 0.5 m/s to 1.0 m/s (Mistakidis, 1956; Jones et al., 2000; Davies et al., 2009).  In the southern North Sea close to the coast of England, Sabellaria spinulosa reefs have been recorded in areas exposed to peak spring tidal flows of 1.0 m/s (Pearce et al., 2014). Davies et al. (2009) also found, through laboratory experiments with Sabellaria spinulosa in tanks, that increasing the water flow to an average of 0.03 m/s is adequate to begin distribution of the sediment rain from the airlift throughout the tank and that doubling the water flow to almost 0.07 m/s further improved particle distribution throughout the tank.  Therefore, it is likely that Sabellaria spinulosa requires habitats with a water flow above 0.07 m/s so that particles are suspended and distributed for the use of tube building and feeding. 

    Tillin (2010) used logistic regression to develop statistical models that indicate how the probability of occurrence of the congener Sabellaria alveolata changes over environmental gradients within the Severn Estuary.  The model predicted response surfaces were derived for each biotope for each of the selected habitat variables, using logistic regression.  From these response surfaces the optimum habitat range for each biotope could be defined based on the range of each environmental variable where the probability of occurrence, divided by the maximum probability of occurrence, is 0.75 or higher.  These results identify the range for each significant variable where the habitat is most likely to occur.  The modelled ranges should be interpreted with caution and apply to the Severn Estuary alone (which experiences large tidal ranges, high currents and extremely high suspended sediment loads and is therefore distinct from many other estuarine systems).  However, these ranges do provide some useful information on environmental tolerances.  The models indicate that for subtidal Sabellaria alveolata the maximum optimal current speed (the range in which it is most likely to occur) ranges from 1.26-2.46 m/s and the optimal mean current speed ranges from 0.5-1.22 m/s.  Although not directly applicable to Sabellaria spinulosa this data suggests that tube-building Sabellariids can occur within a broad range of current speeds. In cases of reduced water flow, Sabellaria spinulosa is likely to suffer a reduction in the supply of suspended food and particles that are integral for growth and repair.  A long-term decrease in water flow may reduce the viability of populations by limiting growth and tube building but no evidence was found for threshold levels relating to impact.

    Sensitivity assessment. The IR.MIR.KR.Lhyp and CR.MCR.CSab biotopes and sub-biotopes are characteristic of moderate energy environments due to moderate or greater wave action or strong to weak tidal flow, depending on which source of water movement is dominant in any particular site. This biotope IR.MIR.KR.Lhyp.Sab biotope is found in weak tidal flow but moderate wave exposure, which keeps the sand in suspension.  A significant decrease in water flow might reduce the suspension of sand to the detriment of the Sabellaria crusts but benefit red algae, whereas a significant increase in water flow may increase scour to the detriment of the red algal understorey and possibly kelp recruitment but benefit the Sabellaria spinulosa.  Nevertheless, wave action is the dominant source of water movement in this biotope and 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 structure of the biotope, especially as both kelp and red algal dominated biotopes and Sabellaria crusts occur in moderately strong (0.5-1.5 m/s) and strong water flows (1.5-3 m/s).  Therefore, resistance to the pressure is assessed as ‘High’, and resilience ‘High’ so that the sensitivity of this biotope to changes in water flow is assessed as ‘Not Sensitive’ at the benchmark level.   

    Low Medium Medium
    Q: Low
    A: NR
    C: NR
    Q: Medium
    A: Medium
    C: Medium
    Q: Low
    A: Low
    C: Low

    The upper limit of the Laminaria hyperborea bed is determined by wave action, 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), 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., 1998b). Hence, an increase in emergence could lead to mortality of exposed Laminaria hyperborea and the associated habitat. However, a decrease in 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. Sabellaria spinulosa crusts are most abundant in the subtidal (e.g. CR.MCR.CSab) but crusts can occur in the lower intertidal. 

    Sensitivity assessment. Shallow examples of the biotope may lose a proportion of the Laminaria canopy due to an increase in emergence whereas an increase in emergence due to increase water depth might also limit the deeper extents of the Laminaria canopy. Therefore, resistance to the pressure is assessed as ‘Low’, and resilience ‘Medium’ so that the sensitivity of this biotope to changes in emergence is assessed as ‘Medium’.

    High High Not sensitive
    Q: Low
    A: NR
    C: NR
    Q: High
    A: High
    C: High
    Q: Low
    A: Low
    C: Low

    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 to 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 & 2 m 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 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 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. Laminaria 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 sublittoral to a depth of 15 m (Birket et al., 1998b). 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).

    No direct evidence was found to assess this pressure on Sabellaria spinulosa crusts or reefs. 

    Sensitivity assessment. The IR.MIR.KR.Lhyp and CR.MCR.CSab biotopes and sub-biotopes are characteristic of moderate energy environments due to moderate or greater wave action or strong to weak tidal flow, depending on which source of water movement is dominant in any particular site. This biotope IR.MIR.KR.Lhyp.Sab biotope is found in weak tidal flow but moderate wave exposure, which keeps the sand in suspension.  A significant decrease in wave action could reduce the suspension of sand to the detriment of the Sabellaria crusts but benefit red algae, whereas a significant increase in wave action could increase scour to the detriment of the red algal understorey and possibly kelp recruitment but benefit the Sabellaria spinulosa.  Nevertheless, a change in nearshore significant wave height >3% but <5% is unlikely to have a significant effect in areas subject to moderate wave exposure.  Therefore, resistance to the pressure is assessed as ‘High’, and resilience ‘High’ so that the sensitivity of this biotope to changes in water flow is assessed as ‘Not Sensitive’ at the benchmark level.  

    Chemical Pressures

    Use / to open/close text displayedResistanceResilienceSensitivity
    Not Assessed (NA) Not assessed (NA) Not assessed (NA)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    This pressure is Not assessed but evidence is presented where available.
    Not Assessed (NA) Not assessed (NA) Not assessed (NA)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    This pressure is Not assessed but evidence is presented where available.
    Not Assessed (NA) Not assessed (NA) Not assessed (NA)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    This pressure is Not assessed but evidence is presented where available.
    No evidence (NEv) Not relevant (NR) No evidence (NEv)
    Q: NR
    A: NR
    C: 
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    No evidence
    Not Assessed (NA) Not assessed (NA) Not assessed (NA)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    This pressure is Not assessed but evidence is presented where available.
    High High Not sensitive
    Q: Low
    A: NR
    C: NR
    Q: High
    A: High
    C: High
    Q: Low
    A: Low
    C: Low

    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).  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 2 mg/l (Cole et al., 1999). No information was found regarding Sabellaria spinulosa tolerance to changes in oxygenation. 

    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 assessed as ‘High’, and the biotope is assessed as ‘Not sensitive’ at the benchmark level.

    Not relevant (NR) Not relevant (NR) Not sensitive
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR

    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 have 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 to 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.

    No direct evidence was found of the effects of nutrient enrichment on Sabellaria spinulosa crusts and reefs. However, this biotope is considered to be 'Not sensitive' at the pressure benchmark, that assumes compliance with good status as defined by the WFD.

    Medium High Low
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium

    Holt et al. (1995) suggest that Laminaria hyperborea may be tolerant of organic 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 have 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 is associated with reduced numbers of perennial macrophytes (Fletcher, 1996). Increased nutrients may also result in phytoplankton blooms that increase turbidity. Therefore, although organic enrichment may not affect kelps directly, indirect effects such as turbidity may significantly affect the structure of Laminaria hyperborea biotopes.

    Sabellaria spinulosa was reported to show enhanced growth adjacent to a sludge dumping area in Dublin Bay (Walker & Rees 1980).  Hence, Sabellaria spinulosa reef biotopes are probably resistant to a high level of organic enrichment.  Information on the levels of organic matter in Dublin Bay was not provided and so it is unclear how the levels experienced relate to the pressure benchmark. Sabellaria spinulosa reefs are found in areas of high water movement of up to 1 m/s (Pearce et al., 2014) that would naturally disperse some organic matter preventing accumulation and siltation.  In larger, dense colonies of Sabellaria spinulosa, sand, detritus, and finer faecal materials collect in between worm tubes.  These detritus layers do not interrupt the normal growth of the individuals or the colony as a whole (Schafer, 1972).  Hence, it seems likely that Sabellaria spinulosa crusts and reefs are resistant to the deposition of a fine layer of organic materials.

    Indirect effects arising from inputs of organic matter are possible where habitat quality and species interactions are altered.  In the Wadden Sea, large subtidal areas of Sabellaria spinulosa reefs have been completely lost since the 1920s.  This decline was partly attributed to an increase in coastal eutrophication that favoured blue mussel beds (Dörjes, 1992; Hayward & Ryland, 1998; Benson et al., 2013).  However, a direct causal link has not been established and it is possible that the decline of Sabellaria spinulosa reefs was due to physical damage from fishing activities rather than competitive interactions (Jones et al., 2000).

    Sensitivity assessment. Little evidence was found to support this sensitivity assessment. Sabellaria spinulosa and the associated species assemblage (which typically includes attached filter feeders from several phyla) is likely to be able to consume extra organic matter.  This conclusion is supported by the enhanced growth rates recorded in the vicinity of sewage disposal areas (Walker & Rees, 1980). However, the Laminaria canopy and especially epiphytes and red algal epiflora may experience a reduction in abundance due to increased turbidity and competition with opportunistic green algae. Therefore, resistance is assessed as 'Medium' as a precaution, albeit with 'Low' confidence. Hence, resilience is assessed as 'High' and the sensitivity of this biotope as 'Low'.

    Physical Pressures

    Use / to open/close text displayedResistanceResilienceSensitivity
    None Very Low High
    Q: High
    A: High
    C: High
    Q: High
    A: High
    C: High
    Q: High
    A: High
    C: High
    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 Very Low High
    Q: High
    A: High
    C: High
    Q: High
    A: High
    C: High
    Q: High
    A: High
    C: High

    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 (Birkett et al., 1998b). Sabellaria spinulosa also develops crusts and reefs on coarse sediment and could probably recover.  However, the biotope would no longer be a rock habitat, would lose its macroalgal component and be lost. Therefore, resistance to the pressure is assessed 'None' and resilience 'Very Low' so that sensitivity is assessed as 'High'.

    Not relevant (NR) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Not relevant on hard rock habitats
    Not relevant (NR) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Not relevant on hard rock habitats
    Low Medium Medium
    Q: High
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium

    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 one metre off the seabed. The associated holdfast communities recovered in six years, however, the epiphytic stipe community did not fully recover within the same 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 the time of year the blocks were cleared. However, the blocks were dominated by Laminaria hyperborea within two years of clearance. Leinaas & Christie (1996) also observed Laminaria hyperborea re-colonization of 'urchin barrens', following the removal of urchins. The substratum was initially colonized by filamentous macroalgae and Saccharina latissima but Laminaria hyperborea dominated the community after 2-4 years.

    Sabellaria spinulosa reef biotopes are directly exposed to physical damage that affects the surface. Gibb et al. (2014) found no direct evidence for impacts of the surface only for Sabellaria spinulosa.  Studies of intertidal reefs of the congener Sabellaria alveolata (Cunningham et al., 1984)  found that the reef recovered within 23 days from the effects of trampling (i.e. treading, walking or stamping on the reef structures) by repairing minor damage to the worm tube porches.  Severe damage caused by kicking and jumping on the reef structure, resulted in large cracks between the tubes, and removal of sections (ca 15 x15 x10 cm) of the structure (Cunningham et al., 1984).  Subsequent wave action enlarged the holes or cracks.  However, after 23 days, at one site, one side of the hole had begun to repair, and tubes had begun to extend into the eroded area. 

    Vorberg (2000) used video cameras to study the effect of shrimp fisheries on Sabellaria alveolata reefs in the Wadden Sea.  The imagery showed that a 3 m beam trawl easily ran over a reef that rose to 30 to 40 cm, although the beam was occasionally caught and misshaped on the higher sections of the reef.  At low tide, there were no signs of the reef being destroyed and, although the trawl had left impressions, all traces had disappeared four to five days later due to the rapid rebuilding of tubes by the worms.  The daily growth rate of the worms during the restoration phase was significantly higher than undisturbed growth, that is, the growth rate of undisturbed tubes was 0.7 mm/day but after removal of 2 cm of surface it was 4.4 mm/day), which indicated that as long as the reef is not completely destroyed recovery can occur rapidly. 

    Sabellaria spinulosa reefs are thought to be more fragile than Sabellaria alveolata (B. Pearce, pers. comm., cited from Gibb et al., 2014) and, therefore, surface abrasion may lead to greater damage and lower recovery rates than observed for Sabellaria alveolataSabellaria spinulosa reefs are often only approximately 10 cm thick, surface abrasion can, therefore, severely damage and/or remove a reef. No direct observations of reef recovery, through repair, from abrasion were found for Sabellaria spinulosa.

    Sensitivity assessment. Based on the evidence discussed above, abrasion at the surface of Sabellaria spinulosa crusts is likely to damage the tubes and result in sub-lethal and lethal damage to the worms. It is also likely to remove a proportion of the Laminaria canopy, attached epiphytes, Laminaria holdfasts and understorey macroalgae (where present). Therefore, resistance is assessed as ‘Low’ (loss of 25-75% of the extent/abundance of component species within the impact footprint).  Hence, resilience is assessed as ‘Medium’ (within 2-10 years) and sensitivity as ‘Medium’.  

    Not relevant (NR) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Not relevant on hard rock habitats, please refer to pressure 'Abrasion/disturbance of the substratum on the surface of the seabed' above.
    Low Medium Medium
    Q: High
    A: High
    C: Medium
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium

    Suspended Particle Matter (SPM) concentration has a linear relationship with subsurface 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 that determine the depth range of Laminaria hyperborea (0-47 m Below Sea Level) (Birkett et al., 1998b).  Light penetration influences the maximum depth at which kelp species can grow and it has been reported that laminarians grow at depths at which the light levels are reduced to one per cent 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 to 2.5 m (Birkett et al. 1998b), 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 decrease its abundance and density (see IR.HIR.KFaR.LhypR.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 sporophytes growth can occur in light-limited environments (Christie 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. Thus, a decrease in water clarity is likely to decrease the abundance of Laminaria hyperborea in the affected area (Norton, 1978).  The biotope is expected to be excluded from silt rich environments.

    Sabellaria spinulosa do not rely on light penetration for photosynthesis, it is also believed that visual perception is limited and that this species does not rely on sight to locate food or other resources.  In a recent review of the sensitivity of Sabellaira spinulosa reefs to anthropogenic disturbance, Fariñas-Franco et al. (2014) concluded that impacts on Sabellaria spinulosa due to a decrease in water clarity resulting from an increase in suspended solids (inorganic or organic) are unlikely, although no thresholds regarding tolerance or intolerance were found.  Decreases in suspended particles that reduce the supply of food or tube-building materials may, however, negatively impact this species (Davies et al., 2009; Last et al., 2011).

    Sabellaria spinulosa relies on a supply of suspended solids and organic matter to filter feed and build protective tubes and so they are often found in areas with high levels of turbidity.  Davies et al. (2009) and Last et al. (2011) developed Vortex Resuspension Tanks (VoRT)  to test the effects of a change in the composition of suspended sediment on benthic species.  This laboratory experiment manipulated turbidity and current flow and demonstrated the susceptibility of Sabellaria spinulosa to a decrease in suspended particulate matter (SPM).  A clear erosion of tubes was observed in the absence of SPM and subsequent starvation of tube building materials.  At high and intermediate sediment regimes (high SPM ~71 mg/l) conditions were comparable to what might be expected within only a few hundred meters distance of a primary aggregate extraction site and Sabellaria spinulosa maintained a cumulative growth rate at these rates of SPM.  This supports the view that the availability of suspended particles is necessary for Sabellaria spinulosa development and that tolerance of elevated levels is likely (Davies et al., 2009). Indirect evidence for the tolerance of Sabellaria spinulosa for changes in turbidity is provided by the persistence of reefs on the outskirts of aggregate dredging areas (Pearce et al., 2007, 2011a), which appear unaffected by dredging that is likely to have led to sediment plumes.  Such plumes, however, are short-lived (Tillin et al., 2011) and, therefore, the long-term effect depends on the duration of dredging activities.

    Tillin (2010) used logistic regression to develop statistical models that indicate how the probability of occurrence of the congener Sabellaria alveolata changes over environmental gradients within the Severn Estuary. The modelled ranges should be interpreted with caution and apply to the Severn Estuary alone (which experiences large tidal ranges, high currents and extremely high suspended sediment loads and is therefore distinct from many other estuarine systems).  The models indicate that the optimal mean neap sediment concentrations for subtidal Sabellaria alveolata range from 515.7 to 906 mg/l and optimal mean spring sediment concentrations range from 855.3 to 1631 mg/l.  Although not directly applicable to Sabellaria spinulosa this data suggests that tube-building sabellariids are tolerant to very high levels of suspended sediment.  Fine sediments such as mud may clog the gills and feeding tentacles of some polychaetes and, therefore, the potential impact will be mediated by the character of the sediment in suspension.

    Sensitivity assessment. The benchmark for this pressure refers to a change in turbidity of one rank, e.g. from clear (<10 mg/l) to intermediate (10-100 mg/l) or intermediate to medium (100-300 mg/l).  Sabellaria spinulosa do not photosynthesise and do not rely on sight to locate resources and therefore no effects are predicted for reef biotopes from an increase or decrease in clarity resulting from a change in one rank on the water framework directive scale.  Experiments (Davies et al., 2009) and predictive modelling (Tillin, 2010) indicate that tube building sabellariids can tolerate a broad range of suspended solids so the Sabellaria crusts are unlikely to be affected by an increase in suspended sediment. However, if the supply of sand to the habitat was reduced, then the Sabellaria crusts would probably erode and be replaced with a diverse understorey of red algae, similar to IR.MIR.KR.Lhyp.  Similarly, an increase in turbidity will reduce the abundance of the Laminaria hyperborea canopy, especially in deeper examples of the biotope, and the Laminaria may be replaced by Saccharina latissima or by an abundant Sabellaria crust similar to CR.MCR.CSab.Sspi. Overall, the biotope is likely to change in character, be reclassified, and, effectively, lost. Therefore, resistance is assessed as ‘Low’,  resilience as ‘Medium’, and sensitivity is assessed as 'Medium'.

    High High Not sensitive
    Q: High
    A: High
    C: Medium
    Q: High
    A: High
    C: High
    Q: High
    A: High
    C: Medium

    Smothering by sediment (e.g. 5 cm of fine material) in 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 and 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.  However, this biotope is found in sand-laden waters (JNCC, 2015) so that the understorey of red algae and epifauna is limited in abundance.

    Sabellaria spinulosa is often found in areas of high water movement with some degree of sediment transport essential for tube-building and feeding.  Sabellaria spinulosa reefs adjacent to aggregate dredging areas appear unimpacted by dredging operations (Pearce et al., 2007; Pearce et al., 2011a).  Evidence suggests that given the dynamic sedimentary environments in which sabellariids live, their populations can certainly persevere in turbid conditions despite ‘typical’ natural levels of burial (Last et al., 2011) and that recovery from burial events is high. Last et al. (2011) buried Sabellaria spinulosa worms (isolated into artificial tubes), under three different depths of sediment – shallow (2 cm), medium (5 cm) and deep (7 cm).  The results indicated that Sabellaria spinulosa could survive short-term (32 days), periodic, burial by sand of up to 7 cm.  Last et al. (2011) suggested that the formation of ‘emergence tubes’ (newly created tubes extending to the surface) under sediment burial allowed Sabellaria spinulosa to tolerate gradual burial and that perhaps this mechanism allows for continued adult dispersal.  This mechanism occurred most rapidly throughout the 8-day burial at ~1 mm per day (Last et al., 2011).  But even though tube-growth still seems possible under burial, the dumping of fine and coarse material will probably block feeding apparatus and, therefore, worm development will be curtailed.

    Sensitivity assessment. This biotope occurs in moderately wave exposed conditions so that deposited sediments are unlikely to remain for more than a few tidal cycles and the effects of a deposit of 5 cm of fine sediment in a discrete event are likely to be transient. In addition, both Laminaria hyperborea and Sabellaria spinulosa crusts are unlikely to be adversely affected by a light deposition of 5 cm of sediment.   Therefore, resistance to the pressure is assessed as ‘High’, and resilience as ‘High’ so that sensitivity is assessed as ‘Not Sensitive’ at the benchmark level. 

    Low Medium Medium
    Q: High
    A: High
    C: Medium
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium

    Smothering by sediment (e.g. 30 cm of fine material) in a discrete event is unlikely to damage Laminaria hyperborea plants but is likely to affect gametophyte survival, holdfast communities, the epiphytic community at the base of the stipe, 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 and 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 1 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.  However, this biotope is found in sand-laden waters (JNCC, 2015) so that the understorey of red algae and epifauna is limited in abundance.

    Sabellaria spinulosa is often found in areas of high water movement with some degree of sediment transport essential for tube-building and feeding. Sabellaria spinulosa reefs adjacent to aggregate dredging areas appear unimpacted by dredging operations (Pearce et al., 2007; Pearce et al., 2011a).  Evidence suggests that the dynamic sedimentary environments in which sabellariids live, their populations can persevere in turbid conditions in spite of ‘typical’ natural levels of burial (Last et al., 2011) and that recovery from burial events is high.  The congener Sabellaria alveolata was reported to survive short-term burial for days and even weeks in the south-west as a result of storms that altered sand levels up to two meters, although they were, killed by longer-term burial (Earll & Erwin 1983).

    Last et al. (2011) buried Sabellaria spinulosa worms (isolated into artificial tubes), under three different depths of sediment – shallow (2 cm), medium (5 cm) and deep (7 cm).  The results indicate that Sabellaria spinulosa can survive short-term (32 days), periodic burial by sand of up to 7 cm.  Last et al. (2011) suggested that the formation of ‘emergence tubes’ (newly created tubes extending to the surface) under sediment burial allowed Sabellaria spinulosa to tolerate gradual burial and that perhaps this mechanism allows for continued adult dispersal.  This mechanism occurred most rapidly throughout the 8-day burial at ~1 mm per day (Last et al., 2011) but even though tube-growth still seems possible under burial, it is likely that the dumping of fine and coarse material will block feeding apparatus and, therefore, worm development will be curtailed. 

    A Sabellaria spinulosa reef off the coast of Dorset showed periodic burial from large sand waves (Collins, 2003).  The displacement of some colonies that had established themselves on a gas pipeline 1 km off the coast of Aberdeen was also associated with burial (Mistakidis, 1956; cited by Holt et al., 1998).  Furthermore the loss of a 2 km2 area of Ross worm reef in Jade Bay, North Sea was attributed to burial as a consequence of mud deposition, although fishing activity may have contributed to the decline (Dörjes, 1992, cited from Hendrick et al., 2011). The evidence above suggests that Sabellaria spinulosa reefs are sensitive to damage from siltation events (Hendrick et al., 2011).  However, recovery is likely to be rapid given that larval dispersal is not interrupted and new reefs are likely to be able to establish themselves over old buried ones as postulated by (Fariñas-Franco et al., 2014).

    Sensitivity assessment. No direct evidence was found for the length of time that Sabellaria spinulosa can survive beneath 30 cm of sediment.  Although this biotope occurs in moderate energy habitats (due to wave action), deposition of 30 cm of sediment represents a large volume of material that would probably remain for a number of tidal cycles and is expected to damage understorey flora/fauna as well as juvenile Laminaria hyperborea.   Similarly, burial to Sabellaria crusts to a depth 30 cm of fine sediment may also result in loss the abundance or extent of the crusts, based on the observations in Hendrick et al. (2011).  Therefore, as a precautionary assessment, resistance is assessed as ‘Low’ due to the depth of overburden. Hence, resilience is assessed as ‘Medium’ (2-10 years) and sensitivity as ‘Medium’.  

    Not Assessed (NA) Not assessed (NA) Not assessed (NA)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Not assessed.
    No evidence (NEv) Not relevant (NR) No evidence (NEv)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    No evidence
    Not relevant (NR) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Not relevant
    Low Medium Medium
    Q: Low
    A: NR
    C: NR
    Q: Medium
    A: Medium
    C: Medium
    Q: Low
    A: Low
    C: Low

    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.

    Not relevant (NR) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    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) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Not relevant. Collision from grounding vessels is addressed under abrasion above.
    Not relevant (NR) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Not relevant

    Biological Pressures

    Use / to open/close text displayedResistanceResilienceSensitivity
    Not relevant (NR) Not relevant (NR) Not relevant (NR)
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    Q: NR
    A: NR
    C: NR
    None of the important structuring characteristic species (e.g. Laminaria hyperborea or Sabellaria spinulosa) are subject to genetic modification or translocation, at present. Therefore, this pressure is considered 'Not relevant'
    Low Very Low High
    Q: High
    A: Low
    C: Medium
    Q: High
    A: High
    C: High
    Q: High
    A: Low
    C: Medium

    The oyster drill, Urosalpinx cinerea, is not known to predate on polychaetes (Brown & Richardson, 1988), therefore, their introduction is not considered a threat to Sabellaria spinulosa. There is, however, some overlap between the environmental niche of Sabellaria spinulosa and the oysters that Urosalpinx cinerea selectively feed on (Brown & Richardson, 1988).  Japanese wireweed Sargassum muticum and green sea fingers Codium fragile have the potential to compete for space where Sabellaria spinulosa reefs occur intertidally, however, intertidal biotopes are not included in this assessment and these species are unlikely to impact deeper subtidal reefs. The assessed biotope occurs in areas of high turbidity and the associated fauna tend to be scour tolerant so that wireweed and green sea fingers would probably be excluded. 

    No records of the carpet sea squirt Didemnum vexillum, the reef building serpulid Ficopomatus enigmaticus, the colonial sea squirt Perophora japonica, or Japanese kelp Undaria pinnatifida, suggest these species occur on or near Sabellaria spinulosa reefs. However, the further spread may impact subtidal Sabellaria spinulosa reefs through smothering or competition, although this is entirely speculative. The assessed biotope supports a variety of attached epifauna including species of bryozoans, hydroids and sponges so the stalked sea squirt Styela clava may be able to colonize this biotope but is unlikely to have greater negative impacts than native species.

    Two species that potentially pose a threat to Sabellaria spinulosa reefs or crusts are the Pacific oyster Magallana gigas and the slipper limpet Crepidula fornicata. Reefs of Sabellaria alveolata in the bay of Mont Saint Michel, France are becoming increasingly colonized by the pacific oyster Magallana gigas (Dubois et al. 2006). Given the high filtration rates of Magallana gigas, it is believed that they can out-compete Sabellaria alveolata for feeding resources (Dubois et al., 2006). In the Wadden Sea, Magallana gigas has replaced blue mussels (Foster-Smith, 2000) suggesting that Magallana gigas may impact filter-feeding, reef-forming organisms in general. The reasons underlying the species shift from Mytilus edulis to Magallana gigas have not been elucidated, however, and may be due to recent changes in climatic conditions (Thieltges, 2005) rather than competitive interactions. It should be noted that even though Magallana gigas is distributed throughout UK waters following an initial introduction in 1926 (Linke, 1951) there is currently no evidence, in the absence of any targeted studies, that this species is impacting native Sabellaria spinulosa or Sabellaria alveolata reefs (Hendrick, et al. 2011).

    When the slipper limpet Crepidula fornicata settles in an area it can increase the amount of pseudofaeces and subsequently the substratum may be altered from hard substratum to soft sediment which will reduce the substratum available for settlement by other species. This was observed when a 28-30% mortality of Mytilus edulis occurred after the introduction of Crepidula fornicata to mussel beds (Thieltges, 2005). Crepidula fornicata has been recorded in association with Sabellaria spinulosa reefs at Hastings Shingle Bank (up to 66 individuals per grab, Pearce et al., 2007) and in lower numbers in the East Coast REC area (maximum 4 per grab (Pearce et al.,  2011a)). The relationship between Crepidula fornicata and Sabellaria spinulosa has not been investigated. However, potential impacts on Sabellaria spinulosa reefs and the associated epifauna could occur through changes to substratum suitability or other interactions.

    However, Undaria pinnatifida has received a large amount of research attention as a major Invasive Non-Indigenous Species (INIS) which could out-compete native UK kelp habitats (see Farrell & Fletcher, 2006; Thompson & Schiel, 2012, Brodie et al., 2014; Hieser et al., 2014). Undaria pinnatifida was first recorded in Plymouth Sound, UK in 2003 (NBN, 2015) subsequent surveys in 2011 have reported that Undaria pinnatifida is widespread throughout Plymouth Sound, colonizing rocky reef habitats. Where Undaria pinnatifida is present there was a significant decrease in the abundance of other Laminaria species, including Laminaria hyperborea (Heiser et al., 2014). In New Zealand, Thompson & Schiel (2012) observed that native fucoids could out-compete Undaria pinnatifida and re-dominate the substratum.  However, Thompson & Schiel (2012) suggested the fucoid recovery was partially due to an annual Undaria pinnatifida die back, which as noted by Heiser et al. (2014) did not occur in Plymouth Sound, UK. It is unknown whether Undaria pinnatifida will out-compete native macroalgae in the UK. However, from 2003-2011 Undaria pinnatifida had spread throughout Plymouth Sound, UK, becoming a visually dominant species at some locations within summer months (Hieser et al., 2014). While Undaria pinnatifida may replace Laminaria hyperborea in some locations within the UK, at the time of writing there is limited evidence available to assess what ecological impacts this invasion may have on Laminaria hyperborea associated communities e.g. red seaweeds.

    Undaria pinnatifida was successfully eradicated on a sunken ship in Clatham 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 Farrell & Fletcher (2006) once established Undaria pinnatifida resists most attempts of long-term removal. The biotope is unlikely to fully recover until Undaria pinnatifida is fully removed from the habitat, which, is unlikely.

    Sensitivity assessment. No evidence was found that non-indigenous species are currently significantly impacting Sabellaria spinulosa reef biotopes but Crepidula fornicata and Magallana gigas may pose a potential threat in terms of competition for food and space and so this assessment may require updating in the future as the distributions and interactions between these species are better understood. However, Undaria pinnatifida has the potential to out-compete Laminaria hyperborea and change the character (and classification) of the biotope. Therefore, resistance is assessed as ‘Low’ and resilience as ‘Very Low’ so that the sensitivity of this biotope to the introduction of INIS is assessed as ‘High’.

    Medium High Low
    Q: Low
    A: NR
    C: NR
    Q: Medium
    A: Medium
    C: Medium
    Q: Low
    A: Low
    C: Low

    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). The 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). However, no evidence was found for adverse impacts of microbial pathogens on Sabellaria spinulosa.   Therefore, resistance to the pressure is assessed as ‘Medium’, based on the possible effects on Laminaria hyperborea. However, resilience is probably ‘High’ so that sensitivity is assessed as ‘Low’.

    None Medium Medium
    Q: High
    A: High
    C: Medium
    Q: Medium
    A: Medium
    C: Medium
    Q: Medium
    A: Medium
    C: Medium

    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 one metre off the seabed. The associated holdfast communities recovered in six years, however, the epiphytic stipe community did not fully recover within the same 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 the time of year the blocks were cleared.  However, within 2 years of clearance, the blocks were dominated by Laminaria hyperborea. Leinaas & Christie (1996) observed Laminaria hyperborea re-colonization of “urchin barrens”, following removal of urchins. The substratum was initially colonized by filamentous macroalgae and Saccharina latissima but Laminaria hyperborea dominated the community after 2-4 years. Following disturbance or in areas were recurrent rapid disturbance occurs Laminaria hyperborea recruitment could also be affected by interspecific 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. Sabellaria spinulosa has no economic value and is not commercially harvested and itself is not directly impacted by this pressure. 

    Sensitivity assessment. Therefore, resistance is assessed as ‘None’, and resilience ‘Medium’ so that the sensitivity of this biotope to the removal of target species is assessed as ‘Medium’.

    Low Medium Medium
    Q: Low
    A: NR
    C: NR
    Q: Medium
    A: Medium
    C: Medium
    Q: Low
    A: Low
    C: Low

    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 2-3 years of harvesting, a new canopy had formed one metre off the seabed. The associated holdfast communities recovered in six years, however, the epiphytic stipe community did not fully recover within the same 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 the time of year the blocks were cleared.  However, the blocks were dominated by Laminaria hyperborea within two years of clearance. Leinaas & Christie (1996) observed Laminaria hyperborea re-colonization of 'urchin barrens', following the removal of urchins. The substratum was initially colonized by filamentous macroalgae and Saccharina latissima but Laminaria hyperborea dominated the community after 2-4 years. Following disturbance or in areas were recurrent rapid disturbance occurs Laminaria hyperborea recruitment could also be affected by interspecific 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. 

    Sabellaria spinulosa biotopes may be removed or damaged by static or mobile gears that target other species. These direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures. Evidence for ecological interactions between Sabellaria spinulosa and other species is limited. The removal of Sabellaria spinulosa predators as by-catch may be beneficial. Sabellaria spinulosa reefs appear to be important nursery areas for commercially targeted flatfish including Dover sole (Bryony Pearce, pers comm). Assessment of this indirect effect is limited by the lack of empirical evidence for predator-prey relationships. Stomach analysis of fish by Pearce (2001) found that juvenile flatfish captured in reef areas including Dover sole, dab and plaice fed preferentially on Sabellaria spinulosa. Pearce et al. (2011b) found that butterfish Pholis gunnellus and dragonet Callionymus lyra also prey on Sabellaria spinulosa. Previous studies have also shown that Carcinus maenas feeds on Sabellaria spinulosa (Taylor, 1962; Bamber & Irving, 1997). Other invertebrates such as Pandalus montagui and Asterias rubens found in association with Sabellaria spinulosa reefs may also be feeding on the worms or other species associated with the reefs rather than Sabellaria spinulosa. Due to the limited information available on predator-prey relationships, the impact of predator removal on Sabellaria spinulosa reef biotopes cannot be assessed.  Dense aggregations of the brittle star, Ophiothrix fragilis, have been suggested to compete with Sabellaria spinulosa for space and food and potentially to consume the gametes inhibiting recruitment (George & Warwick 1985). Removal of this species as by-catch could potentially be beneficial to the reef biotopes.

    Sensitivity assessment. Although the removal of predatory species by commercial fisheries may be beneficial to Sabellaria spinulosa, the accidental removal (e.g. as by-catch) of a proportion of the kelp bed and possibly the Sabellaria spinulosa crusts could impact the biotope. Therefore, resistance is assessed as 'Low' and resilience as ‘Medium’ so that sensitivity is assessed as 'Medium’.

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    Citation

    This review can be cited as:

    Hill, J.M., Tillin, H.M., Marshall, C. & Gibb, N., 2020. [Sabellaria spinulosa] with kelp and red seaweeds on sand-influenced 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 21-10-2020]. Available from: https://www.marlin.ac.uk/habitat/detail/144

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    Last Updated: 21/02/2020