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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

Saccharina latissima with Phyllophora spp. and filamentous green seaweeds on variable or reduced salinity infralittoral rock

08-11-2016

Summary

UK and Ireland classification

UK and Ireland classification

Description

Shallow infralittoral bedrock or boulder slopes, in reduced or low salinity conditions, characterized by the kelp Laminaria saccharina with dense stands of silted filamentous green seaweeds and red seaweeds Phyllophora crispa, Phyllophora pseudoceranoides and Phycodrys rubens. The filamentous green seaweeds e.g. Chaetomorpha melagonium and Cladophora spp. can form a blanket cover amongst the Laminaria saccharina in the upper zone, which is under greater influence of freshwater input. In deeper water the green seaweeds are replaced by red seaweed Phyllophora spp. or Polysiphonia fucoides which may form a distinct sub-zone in the biotope. Coralline crusts can be present. The solitary ascidians Corella parallelogramma and Ascidiella scabra are often epiphytic on the seaweed (particularly Phyllophora spp.) and dominate the animal community along with the starfish Asterias rubens. The small ascidian Dendrodoa grossularia, the barnacle Balanus crenatus and the tube-building polychaete Spirobranchus (syn. Pomatoceros) triqueter occur on the rock surface. More mobile species include the crab Carcinus maenas, the hermit crab Pagurus bernhardus and the whelk Buccinum undatum. Bryozoans Electra pilosa and Spirorbis sp. may cover kelp fronds. The red seaweed Odonthalia dentata may be present in the north. (Taken from Connor et al., 2004).

Depth range

0-5 m, 5-10 m

Additional information

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Further information sources

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Sensitivity reviewHow is sensitivity assessed?

Sensitivity characteristics of the habitat and relevant characteristic species

IR.LIR.KVS.Cod, IR.LIR.KVS.LsacPhyVS & IR.LIR.KVS.LsacPsaVS are within the “Kelp in Variable or Reduced Salinity” habitat complex (IR.LIR.KVS), which are predominantly shallow low energy biotopes found in areas of low or reduced salinity typically in Scotland but also in other sheltered locations around the British Isles e.g. harbours. IR.LIR.KVS.Cod is characterized by dense stands of Codium spp., silt tolerant red seaweeds and sparse Saccharina latissima (syn. Laminaria saccharina). IR.LIR.KVS.LsacPsaVS is characterized by Saccharina latissima but intense Psammechinus miliaris grazing combined with low salinity maintains low biodiversity, resulting in an understory community of depauperate coralline-encrusted rock with predominantly grazing resistant or mobile fauna e.g. Pomotoceros spp. IR.LIR.KVS.LsacPhyVS is characterized by Saccharina latissima with dense stands of silted filamentous green seaweeds and red seaweeds; Phyllophora crispa, Phyllophora pseudoceranoides and Phycodrys rubens.

In undertaking this assessment of sensitivity, an account is taken of knowledge of the biology of all characterizing species in the biotope. For this sensitivity assessment Codium spp., Saccharina latissima represent the dominant characterizing algae, and Psammechinus miliaris represent urchin grazers are the primary foci of research, it is recognized that the understory red seaweed communities of IR.LIR.KVS.Cod and IR.LIR.KVS.LsacPhyVS also define these biotopes. Examples of important species groups are mentioned where appropriate.

The biotopes IR.LIR.KVS biotope complex is distinguished by the relative abundance or Saccharina latissima, and Codium sp, the diversity of red and brown algae that ranges between low salinity or scour tolerant species, and presence or absence of grazers.  The sensitivity of the dominant kelp and red algae are probably consistent for most of the pressures assessed. Therefore, except where indicated, all assessments are considered to apply to all the biotopes within the biotope complex.

Resilience and recovery rates of habitat

There are four species of Codium spp. and two sub-species in the UK; Codium fragile subsp. atlanticum, Codium fragile subsp. tomentosoides, Codium bursa, Codium tomentosum and Codium vermilaria (Silva, 1955; Bunker et al., 2012). IR.LIR.KVS.Cod does not specifically refer to 1 (sub) species as characteristic, therefore, evidence used within this assessment has been sourced from literature cover all 6 species and subspecies. Codium spp. has a perennial life strategy (Bulleri & Airoldi, 2005). Viable zoospores can be produced in the first year of growth from June to autumn (Churchill & Moeller, 1972), spores then germinate and germlings persist through winter undergoing rapid thalli growth when water temperature increases the following spring/summer (Haniask, 1979; Bulleri & Airoldi, 2005). In successive years, the thalli can fragment during winter reducing individuals to a holdfast which may then persist throughout the winter (Fralick & Methieson, 1972), in early spring (April-May) a new frond will develop from the holdfast (Trowbridge, 1995, 1996). Codium fragile gametes can settle and germinate on a variety of substrata including rock fractions, as well as shellfish, coralline algae, serpulid casts and solitary ascidians (Bulleri & Airoldi, 2005). Recruitment is, however, strongly influenced by temperature (see below), salinity (see below), wave exposure and the availability of bare space at the time of gamete release (Trowbridge, 1995, 1998, 1999; Bégin & Scheibling, 2003). Fralick & Methieson (1972) suggested cold temperatures caused Codium spp. thalli to fragment and that fragmented sections of Codium were then capable of reattachment to hard substrata by means of colourless filaments which grow from the point of fragmentation. In most cases it took several weeks for re-attachment to occur but in summer fragments could re-attach within 3-6 days.

Saccharina lattisma is a perennial kelp characteristic of wave sheltered sites of the North East Atlantic, distributed from northern Portugal to Spitzbergen, Svalbard (Birkett et al., 1998; Connor et al., 2004; Bekby & Moy, 2011; Moy & Christie, 2012). Saccharina lattisma is capable of reaching maturity within 15-20 months (Sjøtun, 1993) and has a life expectancy of 2-4 years (Parke, 1948). Maximum growth has been recorded in late winter early spring, in late summer and autumn growth rates slow (Parke, 1948; Lüning, 1979; Birkett et al., 1998). The overall length of the sporophyte may not change during the growth season due to the marginal (distal) erosion of the blade, but extension growth of the blade has been measured at 1.1 cm/day, with total length addition of over 2.25m of tissue per year (Birkett et al., 1998). Saccharina latissima has a heteromorphic life strategy. Large numbers of zoospores are released from sori located centrally on the blade between autumn and winter. Zoospores settle onto rock substrata and develop into dioecious gametophytes (Kain, 1979) which, following fertilization, germinate into juvenile sporophytes from winter-spring.  Kelp zoospores are expected to have a large dispersal range, however, 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).

A large pressure for Laminaria hyperborea biotopes (e.g. IR.HIR.KFaR.LhypR) is urchin grazing pressure, particularly from the species Echinus esculentus, Paracentrotus lividus and Strongylocentrotus droebachiensis. Multiple authors (Steneck et al., 2002; Steneck et al., 2004; Rinde & Sjøtun, 2005; Norderhaug & Christie, 2009; Smale et al., 2013) have reported dense aggregations of sea urchins to be a principal threat to Laminaria hyperborea biotopes of the North Atlantic. Intense urchin grazing creates expansive areas known as “urchin barrens”, in which a shift can occur from Laminaria hyperborea dominated biotopes to those characterized by coralline encrusting algae, with a resultant reduction in biodiversity (Leinaas & Christie, 1996; Steneck et al., 2002, Norderhaug & Christie, 2009). Continued intensive urchin grazing pressure on Laminaria hyperborea biotopes can inhibit the Laminaria hyperborea recruitment (Sjøtun et al., 2006) and cause urchin barrens to persist for decades (Christie et al., 1998; Steneck et al., 2004; Rinde & Sjøtun, 2005). A kelp recolonization experiment conducted by Leinaas & Christie (1996) removed Strongylocentrotus droebachiensis from “urchin barrens” and observed a succession effect. It was observed that the substratum was initially colonized by filamentous macroalgae and within 2 weeks Saccharina latissima colonised and persisted for 2 years. However after 2-4 years Laminaria hyperborea dominated the community. Despite Laminaria hyperborea’s eventual dominance within the community Leinaas & Christie (1996) demonstrated that Saccharina latissima can colonize cleared areas rapidly.

In 2002 a 50.7-83 % decline of Saccharina latissima was discovered in the Skaggerak region, South Norway (Moy et al., 2006; Moy & Christie, 2012). Survey results indicated a sustained shift from Saccharina latissima communities to those of ephemeral filamentous algal communities. The reason for the community shift was unknown, but low water movement in wave and tidally sheltered areas combined with the impacts of dense human populations e.g. increased land run-off, was suggested to be responsible for the dominance of ephemeral turf macro-algae. Multiple stressors such as eutrophication, increasing regional temperature, increased siltation and overfishing may also be acting synergistically to cause the observed habitat shift.

Psammechinus miliaris is a sea urchin distributed across the north east Atlantic from Morocco to northern Scandinavia (Mortensen, 1927). In the British Isles, it can occur in dense aggregation within sheltered locations e.g. Scottish sea lochs, and its distribution frequently coincides with that of Saccharina latissima (Kelly, 2000). Psammechinus miliaris grazes on a wide array of algae and encrusting organisms, including live Saccharina latissima (as in IR.LIR.KVS.LsacPsaVS) (Kelly, 2000; Connor et al., 2004). Psammechinus miliaris can reach sexual maturity within the first year, reproduce each successive year, (Elmhirst, 1922) and are reported to live up 10 years (Allain, 1978). Gametogenesis begins in May and spawning usually occurs between June and August. Depending on food availability, planktonic larvae will then typically settle out within 20-21 days.  The gut is fully developed 5-7 days after settlement and juveniles begin grazing (Kelly, 2001).

The red algae Phyllophora crispa & Phyllophora pseudoceranoides which combined with filamentous green seaweeds characterize the understory community of IR.LIR.KVS.LsacPhyVS. Depending on the level of impact, recovery of the turf may occur through repair and regrowth of damaged fronds, regrowth from crustose bases or via recolonization of rock surfaces where all the plant material is removed. Although there are few case studies following recovery some general trends are apparent. All the red algae (Rhodophyta) exhibit distinct morphological stages over the reproductive life history. This phenomenon is known as heterotrichy or heteromorphy and describes cases where the algal thallus consists of two parts; a prostrate creeping system exhibiting apical growth and functioning as a holdfast. The thalli can regrow from these crusts where they remain supporting recovery of the biotope (Mathieson & Burns, 1975; Dudgeon & Johnson, 1992). The basal crusts are perennial, tough, resistant stages that prevent other species from occupying the rock surface and allow rapid regeneration and where these remain they provide a significant recovery mechanism.

Phyllophora sp. are distributed across the North Atlantic, within Europe specifically are recorded from the Bay of Bisacy (Molenaar & Breeman, 1994) up to Trondhiem, Norway (Norwegian Seaweeds, 2015). Phyllophora sp. are perennial plants but blades are lost and regrown each year (Newroth, 1972; Molenaar & Breeman, 1994). Culture experiments demonstrated that the time for Phyllophora pseudoceranoides to reach sexual maturity was highly temperature dependant, When kept at 10 or 5°C Phyllophora pseudoceranoides specimens from Helgoland, Germany and Roscoff, France began sporulation within 3 months. However, there was considerable variation, specimens kept at ≥15°C took ≤30 months to begin sporulation (Molenaar & Breeman, 1994). These observations were conducted within controlled experimental conditions and therefore natural environmental variability is likely to lengthen or possibly shorten the time taken for Phyllophora sp. to begin sporulation however it is likely that in a natural setting Phyllophora pseudoceranoides would reach maturity within 2 years (High resilience). Please note, Although some general trends are apparent. Recovery rates, for example, will be greatly influenced by whether the crust stages remain from which the thalli can regrow. If a high proportion of bases are lost, then recovery will depend on either vegetative regrowth from remaining bases and or the supply of propagules from neighbouring populations. Dispersal is limited and propagule supply will be influenced by site-specific factors, particularly local water transport, resilience would likely take2-10 years (Medium resilience).

Resilience assessment. Saccharina latissima has potentially rapid recovery rates, recovering from Strongylocentrotus droebachiensis ‘urchin Barrens’ appearing after a few weeks (Leinaas & Christie, 1996), and can reach maturity within 15-20 months (Birkett et al., 1998). Codium spp. can produce viable spores within their first year of growth, and annually fragmented sections of thalli can re-attach to hard substrata. Psammechinus miliaris can become sexually mature in its first year. Red seaweeds can potentially recover within a single growing season. Resilience is assessed as ‘High’ where resistance is ‘High’. Where resistance is assessed as ‘Medium’ (loss of <25 % of individuals or cover) and the bases remain then recovery is assessed as ‘High’. Where resistance is assessed as ‘Low’ or ‘None’, and a high proportion of red seaweed bases are lost then recovery will depend on either vegetative re-growth of red seaweeds from remaining bases and propagule supply from neighbouring populations, Resilience would be assessed as ’Medium’.

Hydrological Pressures

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

Churchill and Moeller (1972) suggested the minimum temperature for the formation of reproductive structures in Codium fragile was 12-15°C. Haniask (1979) experimentally measured Codium fragile thalli and sporeling growth over a range of environmental conditions. Maximal thalli growth was recorded at 24°C.  The upper temperature threshold has been recorded at 30°C and no detectable growth occurs at <6°C.

Mortensen (1927) reported Psammechinus miliaris was found in Limfjorden, Denmark where winter water temperatures are regularly just above 0°C (Ursin, 1960). At Psammichinus miliaris southern range edge, Morocco and the Azores (Mortensen, 1927), winter-summer temperatures range from17-21°C (Seatemperature, 2015). The optimal temperature tolerances are therefore likely to be between 0-21°C. Furthermore, Psammichinus miliaris reproduces in waters around the Faeroes where the summer temperatures seldom exceed 11°C (Ursin, 1960).

The temperature isotherm of 19-20°C has been reported as limiting Saccharina latissima geographic distribution (Müller et al., 2009). Gametophytes can develop in ≤23°C (Lüning, 1990) however, the optimal temperature range for sporophyte growth is 10-15 °C (Bolton & Lüning, 1982). Bolton & Lüning (1982) experimentally observed that sporophyte growth was inhibited by 50-70% at 20°C and following 7 days at 23°C all specimens completely disintegrated. In the field Saccharina latissima has shown significant regional variation in its acclimation to temperature changes, for example Gerard & Dubois (1988) observed sporophytes of Saccharina latissima which were regularly exposed to ≥20°C could tolerate these temperatures whereas sporophytes from other populations which rarely experience ≥17°C showed 100% mortality after 3 weeks of exposure to 20°C. Therefore, the response of Saccharina latissima to a change in temperatures is likely to be locally variable.

Andersen et al. (2011) transplanted Saccharina latissima in the Skagerrak region, Norway and from 2006-2009. There was annual variation however high mortality occurred from August-November within each year of the experiment. In 2008 of the original 17 sporophytes 6 survived from March-September (approx. 65 % mortality rate). All surviving sporophytes were heavily fouled by epiphytic organisms (estimated cover of 80 & 100%). Between 1960 and 2009, sea surface temperatures in the region have regularly exceeded 20°C and so has the duration which temperatures remain above 20 °C. High sea temperatures have been linked to the slow growth of Saccharina latissima which is likely to decrease the photosynthetic ability of, and increase the vulnerability of Saccharina latissima to epiphytic loading, bacterial and viral attacks (Anderson et al., 2011). These factors combined with the establishment of annual filamentous algae in Skagerrak, Norway are likely to prevent the establishment of self-sustaining populations in the area (Anderson et al., 2011; Moy & Christie, 2012).

Phyllophora crispa and Phyllophora pseudoceranoides are sensitive to large changes in temperature. Through culture experiments, 30°C was found lethal to Phyllophora pseudoceranoides within 4-12 weeks. At 27°C plants were severely damaged after 3 months but were able to recover when returned to lower temperatures.  Furthermore, temperature was found to control the time at which Phyllophora pseudoceranoides begins sporulation. For example, ≥15°C sporulation occurred at 30 months were as 10 °C sporulation occurred at 8 months (Molenaar & Breeman, 1994).

IR.LIR.KVS.Cod, IR.LIR.KVS.LsacPhyVS & IR.LIR.KVS.LsacPsaVS are distributed throughout the UK (Connor et al., 2004). Northern to southern Sea Surface Temperature (SST) ranges from 8-16°C in summer and 6-13°C in winter (Beszczynska-Möller & Dye, 2013)

Sensitivity assessment. A 2°C increase for one year may impair Saccharina latissima sporophyte growth but otherwise not affect the characterizing species.  A 5°C increase for one month combined with high UK summer temperatures may cause mortality in Saccharina latissima populations that are not acclimated to >20°C. Resistance has been assessed as ‘None’, to reflect the potential mass mortality effect of sudden temperature increases on Saccharina latissima, and resilience as ‘Medium’. Sensitivity has been assessed as ‘Medium’.

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

During winter Codium spp. thalli reduce to a small holdfast and biological activity is reduced (Haniask, 1979). Mortensen (1927) reported Psammechinus miliaris was found in Limfjorden, Denmark where winter temperatures are regularly just above 0°C. Saccharina lattissima has a lower temperature threshold for sporophyte growth at 0°C (Lüning, 1990). Phyllophora pseudoceranoides can tolerate temperatures of -2 and 0°C 3 months (Molenaar & Breeman, 1994).  None of the characterizing species are likely to be adversely affected by a temperature decrease at the benchmark level.

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

None Medium Medium
Q: Low
A: NR
C: NR
Q: High
A: Medium
C: High
Q: Low
A: Low
C: Low

Haniask (1979) reported Codium fragile salinity tolerances are variable, and dependant on temperature. At 24°C thalli growth occurred from 12-42‰, with an optimum from 24-30‰. Gezelius (1962) reported the littoral growth form of Psammechinus miliaris had an optimal salinity range of 20-32 ppt, and the sub-littoral growth form had an optimal salinity tolerance of 26-38 ppt.

Karsten (2007) tested the photosynthetic ability of Saccharina latissima under acute 2 and 5 day exposure to salinity treatments ranging from 5-60 psu. A control experiment was also carried at 34 psu. Saccharina latissima showed high photosynthetic ability at >80% of the control levels between 25-55 PSU. The affect of long term salinity changes (>5 days) or salinity >60 PSU on Saccharina latissima’ photosynthetic ability was not tested.

Phyllophora crispa and Phyllophora pseudoceranoides are widely distributed around the UK in full marine conditions (Bunker et al., 2012).

Sensitivity assessment. IR.LIR.KVS.Cod, IR.LIR.KVSLsacPsaVS & IR.LIR.KVS.LsacPhyVS are only recorded from reduced or low salinity conditions (<18-30 psu). An increase to full salinity (30-40 ‰) may cause declines in Codium fragile growth. Phyllophora is recorded within full marine salinity, however, it may not be sufficiently abundant or be outcompeted by other red seaweeds in full salinity. Therefore, a long term change to full salinity (30-40 ‰) may change the character of the biotope, so that they are replaced by more diverse sheltered rock Saccharina latissima biotopes (e.g. IR.LIR.K.Lsac). Resistance has been assessed as ‘None’, resilience as ‘Medium’. The sensitivity of this biotope to an increase in salinity has been assessed as ‘Medium’.

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

Haniask (1979) reported that at 24°C Codium fragile thalli growth could occur from 12-42‰, with an optimum from 24-30‰. 100% mortality occurred at 6‰ and at 12‰ growth was reduced. At the extremes of Codium fragile temperature tolerance (6 & 30°C) salinity tolerances were restricted, thalli grown at 6°C had a tolerance of 18-36 ‰, and thalli grown at 30°C had a salinity tolerance of 18-48 ‰ (Haniask, 1979). Codium fragile sporelings had narrower salinity and thresholds than mature thalli; Spores did not germinate at <18‰.

Lindahl and Runnström (1929) showed (experimentally) that Psammechinus miliaris from the littoral (Z form) and sub-littoral (S form) had different salinity optima. Gezelius (1962) reported the littoral growth form had an optimal salinity range of 20-32 ppt, whereas the sub-littoral growth form 26-38ppt. Mature examples of the littoral growth form tolerated 15 ppt for a period of 27 days, however, were not able to produce gametes at this salinity.

Karsten (2007) tested the photosynthetic ability of Saccharina latissima under acute 2 and 5 day exposure to salinity treatments ranging from 5-60 psu. A control experiment was also carried at 34 psu. Saccharina latissima showed high photosynthetic ability at >80% of the control levels between 25-55 PSU. Hyposaline treatment of 10-20 PSU led to a gradual decline of photosynthetic ability. After 2 days at 5 PSU, Saccharina latissima showed a significant decline in photosynthetic ability at approx. 30% of control. After 5 days at 5 PSU, Saccharina latissima specimens became bleached and showed signs of severe damage. The affect of long term salinity changes (>5 days) or salinity >60 psu on Saccharina latissima’ photosynthetic ability was not tested. The experiment was conducted on Saccharina latissima from the Arctic, and at extremely low water temperatures (1-5 °C) macroalgae acclimation to rapid salinity changes could be slower than at temperate latitudes. It is, therefore, possible that resident Saccharina latissima of the UK maybe be able to acclimate to salinity changes more effectively.

Sensitivity assessment. IR.LIR.KVS.Cod is recorded in full salinity but probably exposed to reduced (18-30 ppt) conditions (Connor et al., 2004). A salinity decrease to “Low” (<18 ppt) may cause declines in Codium spp. growth and detriment the biotope. As a result, the Codium abundance could fall resulting in the LsacPhyVS biotope. IR.LIR.KVS.LsacPsaVS and IR.LIR.KVS.LsacPhyVS are recorded in ‘reduced’ and ‘low’ salinity, A further reduction in salinity would result in close to freshwater conditions and, however unlikely, would result in loss of the biotopes.  Resistance has been assessed as ‘Low’ and resilience as ‘High’. Therefore, the sensitivity of this biotope to a decrease in salinity has been assessed as ‘High’.

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

Information concerning the effects of increased water flow on Codium spp. or Psammechinus miliaris is limited. IR.LIR.KVS.Cod, IR.LIR.KVS.LsacPhyVS & IR.LIR.KVS.LsacPsaVS are predominantly recorded from sites with very weak to weak tidal streams (Connor et al., 2004).

Peteiro & Freire (2013) measured Saccharina latissima growth from 2 sites, the first had maximal water velocities of 0.3m/sec and the second 0.1m/sec. At site 1, Saccharina latissima had significantly larger biomass than at site 2 (16 kg/m to 12 kg/m respectively). Peteiro & Freire (2013) suggested that faster water velocities were beneficial to Saccharina latissima growth. However, Gerard & Mann (1979) found Saccharina latissima productivity is reduced in moderately strong tidal streams (≤1 m/sec) when compared to weak tidal streams (<0.5 m/sec). Despite the results published in Gerard & Mann (1979) Saccharina latissima can characterize or be a dominant in the tide swept biotopes IR.MIR.KT.XKTX & IR.MIR.KT.LsacT, which have been recorded from very strong (>3 m/sec) to moderately strong tidal streams (≤1 m/sec) (Connor et al., 2004), indicating Saccharina latissima can tolerate greater tidal streams than <1m/sec.

Sensitivity assessment. IR.LIR.KVS.Cod, IR.LIR.KVS.LsacPhyVS & IR.LIR.KVS.LsacPsaVS are classed as low energy biotopes, restricted to only weak tidal streams. Many of the characteristic species are found in a range of tidal regimes so that a change in flow velocities of between 0.1-0.2 m/sec would not cause a significant effect on most species present. In LsacCod an increase in water flow at the benchmark may be enough to remove the silt that characterizes the biotope, and allow the abundance of Saccharina latissima to increase. In LsacPsa, an increase in water flow to moderately strong or strong would probably reduce the abundance of Echinus esculentus and to a lesser extent Psammechinus miliaris and favour a change from LsacPsaVS to LsacPhyVS. However, at the benchmark level, there is only likely to be slight changes in the character of the biotope and the KVS complex would remain.

Resistance has been assessed as ‘Medium’, resilience as ‘High’. Sensitivity has been assessed as ‘Low‘at the benchmark level.

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

IR.LIR.KVS.Cod , IR.LIR.KVS.Cod, IR.LIR.KVS.LsacPhyVS & IR.LIR.KVS.LsacPsaVS are predominantly shallow biotopes recorded from 0-10 m BCD An increase in emergence will result in an increased risk of desiccation and mortality of the macro-algae of the biotope.  Removal of canopy-forming kelps, through desiccation, has also been shown to increase desiccation and mortality of the understory macroalgae (Hawkins & Harkin, 1985). Thomsen & McGlathery (2007) demonstrated that Codium fragile biomass declined if artificially placed at higher tidal elevations, and would therefore likely be sensitive to changes in emergence regime. Many of the dominant species an also occur in the lower intertidal, however, the biotope would probably be replaced by a lower shore equivalent.  Providing that suitable substrata are present, the biotope is likely to re-establish further down the shore within a similar emergence regime to that which existed previously.

Sensitivity assessment. Resistance has been assessed as ‘Low’ and resilience  as ‘Medium’. The sensitivity of this biotope to a change in emergence is considered to be ‘Medium’.

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

IR.LIR.KVS.Cod, IR.LIR.KVS.LsacPhyVS & IR.LIR.KVS.LsacPsaVS are classed as low energy biotopes, recorded from sheltered-ultra wave sheltered sites (Connor et al., 2004). Therefore, a large scale increase in wave exposure is likely to have a fundamental effect on the characterizing species. However, evidence that specifically relates to the tolerance of the characterizing species to increases in wave exposure is limited.

Bulleri & Airoldi (2005) recorded the seasonal abundance of Codium fragile on the wave exposed and sheltered faces of breakwaters (coastal defence structures) built in the Adriatic sea. Codium fragile density was similar across both the exposed and sheltered sides in spring-early summer, however as summer progressed Codium fragile density declined on the exposed side of the breakwater. Codium fragile thalli also attained greater sizes (>14 cm) were more branched and had higher biomass on the sheltered faces of the breakwater. Indicating, that wave exposure has an impact on the density of Codium spp. thalli.

At the time of writing there is limited evidence for the effect of wave exposure on Psammechinus miliaris or Saccharina latissima other than they are predominantly recorded in wave sheltered locations (Birkett et al., 1998; Kelly, 2000).

Sensitivity assessment. Wave exposure is one of the principal defining features of rock biotopes, and large changes in wave exposure are likely to alter the relative abundance of the dominant macro-algae, grazing and understory community, and hence, the biotope. However, a change in near shore significant wave height of 3-5% is unlikely to have any significant effect on IR.LIR.KVS.Cod, IR.LIR.KVS.LsacPhyVS or IR.LIR.KVS.LsacPsaVS. Resistance has been assessed as ‘High’, resilience as ‘High’ and sensitivity as ‘Not Sensitive’ at the benchmark level.

Chemical Pressures

 ResistanceResilienceSensitivity
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

Bryan (1984) suggested that the general order for heavy metal toxicity in seaweeds is: organic Hg > inorganic Hg > Cu > Ag > Zn > Cd > Pb. Cole et al. (1999) reported that Hg was very toxic to macrophytes. The effects of copper, zinc and mercury on Saccharina latissima have been investigated by Thompson and Burrows (1984). They observed that the growth of sporophytes was significantly inhibited at 50 µg Cu /l, 1000 µg Zn/l and 50 µg Hg/l. Zoospores were found to be more intolerant and significant reductions in survival rates were observed at 25 µg Cu/l, 1000 µg Zn/l and 5 µg/l.

At the time of writing, little is known about the effects of heavy metals on echinoderms. Bryan (1984) reported that early work had shown that echinoderm larvae were intolerant of heavy metals, e.g. the intolerance of larvae of Paracentrotus lividus to copper (Cu) had been used to develop a water quality assessment. Kinne (1984) reported developmental disturbances in Echinus esculentus exposed to waters containing 25 µg / l of copper (Cu). Sea-urchins, especially the eggs and larvae, are used for toxicity testing and environmental monitoring (reviewed by Dinnel et al. 1988). Taken together with the findings of Gommez & Miguez-Rodriguez (1999) above it is likely that echinoderms are intolerant of heavy metal contamination.

However, this biotope is considered to be 'Not sensitive' at the pressure benchmark, that assumes compliance with all relevant environmental protection standards.

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

Saccharina latissima fronds, being predominantly subtidal, would not come into contact with freshly released oil but only to sinking emulsified oil and oil adsorbed onto particles (Birkett et al., 1998). The mucilaginous slime layer coating of laminariales may protect them from smothering by oil. Hydrocarbons in solution reduce photosynthesis and may be algicidal. However, Holt et al. (1995) reported that oil spills in the USA and from the 'Torrey Canyon' had little effect on kelp forests. Similarly, surveys of subtidal communities at a number sites between 1-22.5 m below chart datum showed no noticeable impacts of the Sea Empress oil spill and clean up (Rostron & Bunker, 1997). An assessment of holdfast fauna in Laminaria showed that although species richness and diversity decreased with increasing proximity to the Sea Empress oil spill, overall the holdfasts contained a reasonably rich and diverse fauna, even though oil was present in most samples (Somerfield & Warwick, 1999).

Echinoderms seem especially sensitive to the toxic effects of oil, likely because of the large amount of exposed epidermis (Suchanek, 1993). Schäfer & Köhler (2009) found 20 day exposure to sub-lethal concentrations of phenanthrene resulted in severe ovarian lesions of Psammechinus miliaris limiting the production of gametes.

Following the Torrey Canyon incident, large numbers of dead Psammechinus miliaris were found in the vicinity of Sennen, UK possibly due to exposure to the oil spill and the heavy spraying of hydrocarbon based dispersants in that area (Smith, 1968). Other significant effects have been observed in other species of urchins. For example, mass mortality of the echinoderm Echinocardium cordatum was observed shortly after the Amoco Cadiz oil spill (Cabioch et al., 1978) and reduced abundance of the species was detectable up to >1000 m away one year after the discharge of oil-contaminated drill cuttings in the North Sea (Daan & Mulder, 1996). In the Mediterranean around Naples, urchins were absent from areas which had visible signs of massive pollution of both sewage and oil. Echinus esculentus populations in the vicinity of an oil terminal in A Coruna Bay, Spain, showed developmental abnormalities in the skeleton. The tissues contained high levels of aliphatic hydrocarbons, naphthalenes, pesticides and heavy metals (Zn, Hg, Cd, Pb, and Cu) (Gommez & Miguez-Rodriguez, 1999). But the observed effects may have been due to a single contaminant or synergistic effects of all present.

Cullinane et al. (1975) found large quantities of Codium fragile washed up on Relane, Bantry Bay, USA shortly after a large oil spill.  No other evidence could be located for the effect of hydrocarbon & PAH contamination on Codium spp.

Sensitivity assessment.  The evidence suggests that echinoderms and Codium spp. are sensitive to hydrocarbon pollution. However, this biotope has been assessed as 'Not sensitive' at the pressure benchmark, that assumes compliance with all relevant environmental protection standards.

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

Johansson (2009) exposed samples of Saccharina latissima to several antifouling compounds, observing chlorothalonil, DCOIT, dichlofluanid and tolylfluanid inhibited photosynthesis. Exposure to Chlorothalonil and tolylfluanid, was also found to continue inhibiting oxygen evolution after exposure had finished, and may cause irreversible damage. Smith (1968) noted that epiphytic and benthic red algae were intolerant of dispersant or oil contamination due to the Torrey Canyon oil spill; only the epiphytes Crytopleura ramosa and Spermothamnion repens and some tufts of Jania rubens survived together with Osmundea pinnatifida, Gigartina pistillata and Phyllophora crispa from the sublittoral fringe. Considerable observations and work, mainly on Echinus esculentus but also on Psammechinus miliaris (Smith, 1968; Gommez & Miguez-Rodriguez, 1999; Dinnel et al., 1988) indicate high intolerance to synthetic contaminants. Newton & McKenzie (1995) state that echinoderms tend to be very intolerant of various types of marine pollution, but there is little more detailed information than this. Following the Torrey Canyon incident, large numbers of dead Psammechinus miliaris in the vicinity of Sennen, UK presumably due to the heavy spraying of dispersants in that area and exposure to the oil spill (Smith, 1968).

However, this biotope is considered to be 'Not sensitive' at the pressure benchmark, that assumes compliance with all relevant environmental protection standards.

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 sensitive
Q: NR
A: NR
C: NR
Q: NR
A: NR
C: NR
Q: NR
A: NR
C: NR

No benchmark was proposed.  Therefore, sensitivity has been assessed as Not sensitive at the pressure benchmark that assumes compliance with all relevant environmental protection standards.

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

Reduced oxygen concentrations can inhibit both photosynthesis and respiration in macroalgae (Kinne, 1977). Despite this, macroalgae are thought to buffer the environmental conditions of low oxygen, thereby acting as a refuge for organisms in oxygen depleted regions especially if the oxygen depletion is short term (Frieder et al., 2012). A rapid recovery from a state of low oxygen is expected if the environmental conditions are transient. If levels do drop below 4 mg/l negative effects on these organisms can be expected, with adverse effects occurring below 2mg/l (Cole et al., 1999).

Under hypoxic conditions, echinoderms become less mobile and stop feeding. The death of a bloom of the phytoplankton Gyrodinium aureolum in Mounts Bay, Penzance in 1978 produced a layer of brown slime on the sea bottom. This resulted in the death of fish and invertebrates, including Echinus esculentus, presumably due to anoxia caused by the decay of the dead dinoflagellates (Griffiths et al., 1979). Spicer (1995) investigated the effects of environmental hypoxia on the oxygen and acid-base status of Psammechinus miliaris. Oxygen uptake is not regulated by this species during progressive hypoxia. The habitat of this species includes rock pools on the shore that can experience quite severe hypoxia or even anoxia. Psammechinus miliaris must be able to tolerate low oxygen conditions provided the event is brief. In prolonged events, subtidal Psammechinus miliaris would presumably react in a similar fashion to the Echinus esculentus above.

Sensitivity Assessment. Reduced oxygen levels are likely to inhibit photosynthesis and respiration but not cause a loss of the macroalgae population directly. Long term de-oxygenation could, however, cause mortality in echinoderms; however intertidal populations of Psammechinus miliaris are likely to be tolerant of hypoxia conditions. Resistance has been assessed as ‘Medium’, Resilience as ‘High’. Sensitivity has been assessed as ‘Low’.

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

Johnston & Roberts (2009) conducted a meta-analysis, which reviewed 216 papers to assess how a variety of contaminants (including sewage and nutrient loading) affected 6 marine habitats (including subtidal reefs). A 30-50% reduction in species diversity and richness was identified from all habitats exposed to the contaminant types. Johnston & Roberts (2009)  also highlighted that macroalgal communities are relatively tolerant to contamination, but that contaminated communities can have low diversity assemblages which are dominated by opportunistic and fast growing species (Johnston & Roberts, 2009 and references therein).

Conolly & Drew (1985) found Saccharina latissima sporophytes had relatively higher growth rates when in close proximity to a sewage outlet in St Andrews, UK when compared to other sites along the east coast of Scotland. At St Andrews, nitrate levels were 20.22 µM, which represents an approx 25% increase when compared to other comparable sites (approx 15.87 µM). Handå et al. (2013) also reported Saccharina latissima sporophytes grew approx 1% faster per day when in close proximity to Norwegian Salmon farms, where elevated ammonium can be readily absorbed.  Read et al. (1983) reported after the installation of a new sewage treatment  works which reduced the suspended solid content of liquid effluent by 60 % in the Firth of Forth, Saccharina latissima became abundant where previously it had been absent.

Haniask (1979) observed that Codium fragile growth rate increased when exposed to elevated nitrogen (Nitrate, Nitrite, Ammonium and Urea). After 21 day nitrogen enrichment treatments Codium fragile grew on average 23-25 mm, whereas in the no enrichment treatment Codium fragile grew 4.8 mm. Conversely Thomsen & McGlathery (2006) observed that short term nutrient enrichment did not increase the biomass of Codium fragile, however, the authors suggested that Codium spp. store excess Nitrogen to sustain growth if nutrients become depleted. Despite disagreement between the authors on the effect of enrichment, in both examples, enrichment did not have a detectable negative impact on Codium spp.

Sensitivity assessment. The evidence suggests that enrichment would not negatively impact on Codium spp. growth or directly affect Saccharina latissima. However indirectly nutrient enrichment may increase turbidity which may decrease water clarity and, therefore, macro-algae photosynthesis. Resistance has therefore been assessed as ‘Medium’, resilience as ‘High’. Sensitivity has been assessed as ’Low’.

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

Johnston & Roberts (2009) conducted a meta-analysis, which reviewed 216 papers to assess how a variety of contaminants (including sewage and nutrient loading) affected 6 marine habitats (including subtidal reefs). A 30-50% reduction in species diversity and richness was identified from all habitats exposed to the contaminant types. Johnston & Roberts (2009) however also highlighted that macroalgal communities are relatively tolerant to contamination, but that contaminated communities can have low diversity assemblages which are dominated by opportunistic and fast growing species (Johnston & Roberts, 2009 and references therein).

Conolly & Drew (1985) found Saccharina latissima sporophytes had relatively higher growth rates when in close proximity to a sewage outlet in St Andrews, UK when compared to other sites along the east coast of Scotland. At St Andrews, nitrate levels were 20.22 µM, which represents an approx 25% increase when compared to other comparable sites (approx 15.87 µM). Handå et al. (2013) also reported Saccharina latissima sporophytes grew approx 1% faster per day when in close proximity to Norwegian Salmon farms, where elevated ammonium can be readily absorbed.  Read et al. (1983) reported after the installation of a new sewage treatment  works which reduced the suspended solid content of liquid effluent by 60% in the Firth of Forth, Saccharina latissima became abundant where previously it had been absent.

Sensitivity assessment. The evidence suggests that enrichment would not negatively impact on Codium spp. growth or directly affect Saccharina latissima. However, indirect organic enrichment may increase turbidity, which may decrease water clarity and therefore negatively effect macroalgal photosynthesis and growth. Resistance has therefore been assessed as ‘Medium’, resilience as ‘High’. Sensitivity has been assessed as ’Low’.

Physical Pressures

 ResistanceResilienceSensitivity
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

This biotope forms on hard rock substrata, i.e. bedrock, boulders and cobbles.  A change from hard rock to sedimentary substrata would result in permanent loss of the biotope. Therefore, resistance is assessed as None, resilience as Very low and sensitivity as High. confidence is assessed as 'High' due to the incontrovertible nature of the pressure.

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 substrata.

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 substrata.

None High Medium
Q: Low
A: NR
C: NR
Q: Medium
A: High
C: High
Q: Low
A: Low
C: Low

Abrasion of the substratum e.g. from bottom or pot fishing gear, cable laying etc. may cause localised mobility of the substrata and mortality of the resident community. The effect would be situation dependent however if bottom fishing gear were towed over a site it may mobilise a high proportion of the rock substrata and cause high mortality in the resident community. Sensitivity assessment. Resistance has been assessed as ‘None’, Resilience as ‘High’. Sensitivity has been assessed 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

Penetration is unlikely to be relevant to hard rock substrata. Therefore, the pressure is Not relevant.  However, physical disturbance of the surface is assessed under 'abrasion' above.

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

Suspended Particle Matter (SPM) concentration has a negative linear relationship with sub-surface light attenuation (Kd) (Devlin et al., 2008). An increase in SPM results in a decrease in sub-surface light attenuation. Light availability and water turbidity are principal factors in determining depth range at which kelp can be found (Birkett et al., 1998). Light penetration influences the maximum depth at which kelp species can grow and it has been reported that laminarians grow at depths at which the light levels are reduced to 1 percent of incident light at the surface. Maximal depth distribution of laminarians, therefore, varies from 100 m in the Mediterranean to only 6-7 m in the silt laden German Bight. In Atlantic European waters, the depth limit is typically 35 m. In very turbid waters the depth at which kelp is found may be reduced, or in some cases excluded completely (e.g. Severn Estuary), because of the alteration in light attenuation by suspended sediment (Lüning, 1990; Birkett et al., 1998).

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 decrease the photosynthetic ability of, abundance and density of Saccharina latissima.

Codium fragile is photosynthetically efficient at low light levels (Ramus et al., 1976). Thomsen & McGlathery (2006) also demonstrated that Codium fragile gained biomass in both low and high light conditions, and found no apparent negative effect of shading on Codium fragile biomass.

Psammechinus miliaris is omnivorous, feeding directly on live and dead algae but also on an array attached fauna (Kelly, 2000). The feeding plasticity of Psammechinus miliaris is likely to ameliorate some of the effects of diminished kelp growth as a result of decreased light availability, however, a decrease in Saccharina latissima may cause some declines in Psammechinus miliaris abundance.

Many red algal species are scour tolerant, and occur in turbid waters and in general algal turfs replace fucoids and kelps in areas where turbidity and sedimentation increase (Airoldi, 2003). Furthermore, many red algal species occur beneath canopies of larger macroalgae (e.g. IR.HIR.KFaR.LhypR) and are tolerant of low light levels (Gantt, 1990).

Sensitivity Assessment. A decrease in turbidity is likely to support enhanced growth (and possible habitat expansion) and is therefore not considered in this assessment. However, an increase in turbidity is likely to result in the loss of Saccharina latissima at the deeper extent of the biotope. Codium spp., Psammechinus miliaris and red algal species are resistant to decreases in water clarity. To represent the potential decline in Saccharina latissima resistance to this pressure has been defined as ‘Medium’ and resilience to this pressure is defined as ‘High’ at the benchmark level due to the scale of the impact. Hence, this biotope is regarded as having a sensitivity of ‘Low‘.

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

Smothering by sediment e.g. 5 cm material during a discrete event, is unlikely to damage Saccharina latissima sporophytes but may affect holdfast fauna, gametophyte survival, interfere with zoospore settlement and, therefore, recruitment processes (Moy & Christie, 2012). Given the short life expectancy of Saccharina latissima (2-4 years-(Parke, 1948)), IR.LIR.KVS.SlatPhyVS is likely to be dependent on annual Saccharina latissima recruitment (Moy & Christie, 2012). Given the microscopic size of the gametophyte, 5 cm of sediment could be expected to significantly inhibit growth. However, laboratory studies showed that kelp gametophytes can survive in darkness for between 6-16 months at 8°C and would probably survive smothering by a discrete event. Once returned to normal conditions the gametophytes resumed growth or maturation within 1 month (Dieck, 1993). Intolerance to this factor is likely to be higher during the peak periods of sporulation and/or spore settlement.

Mature Codium tomentosum thalli can grow up to 30 cm long (Pizzolla, 2007). Therefore, during summer when thalli are erect light deposition of sediment is unlikely to inundate thalli, however if sediment is deposited during winter when the thalli are fragmented and reduced to the holdfast (Haniask, 1979) then Codium spp. thalli will become inundated. It is unknown whether retained sediment would inhibit growth if the holdfast was inundated the following spring.

Psammechinus miliaris is quite small (typically up to 4 cm) and is likely to be inundated by 5 cm of sediment (Jackson, 2008). If unable to 'dig out' of the sediment, deposited sediment may cause mortality.

The effect of deposition of 5cm sediment Phyllophora crispa and Phyllophora pseudoceranoides is likely to be seasonally variable. As highlighted within the resilience section, Phyllophora sp. can lose fronds during winter. Phyllophora crispa fronds can grow to a length of 15cm and Phyllophora pseudoceranoides can grow to a length of 10cm (Bunker et al., 2012). Therefore, if plants are complete deposition is not likely to completely inundate mature individuals. However if sediment deposition occurs during periods of early seasonal thalli growth then this could affect Phyllophora sp. growth.

IR.LIR.KVS.Cod, IR.LIR.KVS.SlatPhyVS and IR.LIR.KVS.SlatPsaVS are classed as low energy habitats, and are therefore unlikely to experience >moderate tidal streams (>0.5 m/sec) or wave action.

Sediment could, therefore, remain within the host habitat and recovery rate would be related to sediment retention but will probably be dissipated within a year. Deposited sediments could affect kelp recruitment (Birkett et al., 1998) and the survival of Psammechinus miliaris.

Sensitivity assessment. SlatCod is a heavily silted biotope (Connor et al., 2004) so an addition of 5 cm of fines may not have a significant effect on the biotope. In SlatPsaVS and SlatPhyV, the deposit of fine sediment may remain for some time (depending on local conditions) and result in the smothering of small invertebrates, and smothering of short turf forming red algae and encrusting corallines.  Smothering would inhibit photosynthesis, growth for algae, and possibly lead to mortality of germlings.  Therefore, a resistance of ‘Medium’ is suggested. Resilience as ‘High’. Sensitivity has been assessed as ‘Low’.

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

Smothering by sediment e.g. 30 cm material during a discrete event, is unlikely to damage Saccharina latissima sporophytes but may affect holdfast fauna, gametophyte survival, interfere with zoospore settlement and, therefore, recruitment processes (Moy & Christie, 2012). Given the short life expectancy of Saccharina latissima (2-4 years (Parke, 1948)), IR.LIR.KVS.SlatPhyVS is likely to be dependent on annual Saccharina latissima recruitment (Moy & Christie, 2012). Given the microscopic size of the gametophyte, 30cm of sediment could be expected to significantly inhibit growth. However, laboratory studies showed that kelp gametophytes can survive in darkness for between 6-16 months at 8°C and would probably survive smothering by a discrete event. Once returned to normal conditions the gametophytes resumed growth or maturation within 1 month (Dieck, 1993). Intolerance to this factor is likely to be higher during the peak periods of sporulation and/or spore settlement.

Mature Codium tomentosum thalli can grow up to 30 cm long (Marlin, 2015). 30cm of deposited sediment is likely to inundate mature thalli. During winter, thalli fragment and individuals are reduced to a holdfast. It is unknown whether retained sediment would inhibit growth if the holdfast was inundated the following spring. 

Psammechinus miliaris is quite small (typically up to 40 mm) and is likely to be inundated by 30 cm of sediment (Jackson, 2008). If unable to 'dig out' of the sediment, deposited sediment may cause mortality.

Phyllophora crispa fronds can grow to a length of 15 cm and Phyllophora pseudoceranoides can grow to a length of 10cm (Bunker et al., 2012). Deposition of 30 cm sediment is likely to completely inundate Phyllophora crispa and Phyllophora pseudoceranoides.

IR.LIR.KVS.Cod, IR.LIR.KVS.SlatPhyVS and IR.LIR.KVS.SlatPsaVS are classed as low energy habitats, and are therefore unlikely to experience >moderate tidal streams (>0.5 m/sec) or wave action.

Sediment could, therefore, remain within the host habitat and recovery rate would be related to sediment retention but will probably be dissipated within a year. Deposited sediments could affect macroalgae recruitment (Birkett et al., 1998) and the survival of Psammechinus miliaris.

Sensitivity assessment Deposition of 30 cm of sediment is likely to inundate all but large macroalgae, e.g. mature Saccharina lattisima, and cause mortality in Codium spp. and understory red seaweeds. As the deposit may remain for some time (depending on local conditions) and mortality is likely. Resistance has been assessed as of ‘None’; resilience has been assessed as ‘Medium’. Sensitivity has been assessed 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

No evidence to suggest that litter would affect kelp and seaweeds was found.

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

No evidence.

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

There is no evidence to suggest that anthropogenic light sources would affect macro-algae. Shading (e.g. by the construction of a pontoon, pier etc) could adversely affect IR.LIR.KVS.Cod, IR.LIR.KVS.SlatPhyVS and IR.LIR.KVS.SlatPsaVS 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 seaweed abundance.

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

 ResistanceResilienceSensitivity
No evidence (NEv) No evidence (NEv) No evidence (NEv)
Q: NR
A: NR
C: NR
Q: NR
A: NR
C: NR
Q: NR
A: NR
C: NR

Saccharina latissima has shown significant regional acclimation to environmental conditions. Gerard & Dubois (1988) found Saccharina latissima sporophytes which were regularly exposed to ≥20°C could tolerate these high temperatures whereas sporophytes from other populations which rarely experience ≥17°C showed 100% mortality after 3 weeks of exposure to 20°C. It is, therefore, possible that transplanted eco-types of Saccharina latissima may react differently to environmental conditions that differ from those of their origin.

However, there was little evidence for translocation of any other characteristic species over significant geographic distances. Nor was there any evidence regarding the genetic modification or effects of translocation.

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

Codium fragile subsp. tomentosoides is a native green alga of Japan which at the time of writing has spread throughout Europe, The Americas, South Africa, Australia and New Zealand. During kelp canopy clearance experiments in Nova Scotia, it was observed that following removal of Laminaria longicruris canopies Codium fragile subsp. tomentosoides can opportunistically colonize cleared patches and inhibit kelp re-colonization (Provan et al., 2005).

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; Heiser et al., 2014). Undaria pinnatifida was first recorded in the UK, Hamble Estuary, in June 1994 (Fletcher & Manfredi, 1995) and has since spread to a number of British ports. Undaria pinnatifida is an annual species, sporophytes appear in Autumn and grow rapidly throughout winter and spring during which they can reach a length of 1.65 m (Birkett et al., 1998). Farrell & Fletcher (2006) suggested that native short lived species that occupy similar ecological niches to Undaria pinnatifida, such as Saccharina latissima, are likely to be worst affected and outcompeted by Undaria pinnatifida. Where present, an abundance of Undaria pinnatifida has corresponded to a decline in Saccharina lattisima (Farrell & Fletcher, 2006) and Laminaria hyperborea (Heiser et al., 2014).

In New Zealand, Thompson and Schiel (2012) observed that native fucoids could out-compete Undaria pinnatifida and re-dominate the substratum. However, Thompson and Schiel (2012) suggested the fucoid recovery was partially due to an annual Undaria pinnatifida die back, which as noted by Heiser et al., (2014) does not occur in Plymouth Sound, UK. 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 Fletcher & Farrell, (1999) once established Undaria pinnatifida resists most attempts at long term removal. The biotope is unlikely to fully recover until Undaria pinnatifida is fully removed from the habitat, which as stated above is unlikely to occur.

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

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

Saccharina latissima may be infected by the microscopic brown alga Streblonema aecidioides. Infected algae show symptoms of Streblonema disease, i.e. alterations of the blade and stipe ranging from dark spots to heavy deformations and completely crippled thalli (Peters & Scaffelke, 1996). Infection can reduce growth rates of host algae.

Psammechinus miliaris is susceptible to 'Bald-sea-urchin disease', which causes lesions, loss of spines, tube feet, pedicellariae, destruction of the upper layer of skeletal tissue and death (Maes et al., 1986). It is thought to be caused by the bacteria Vibrio anguillarum and Aeromonas salmonicida. This disease has been recorded from Psammechinus miliaris from the French Atlantic coast. Although associated with mass mortalities of Strongylocentrotus franciscanus in California and Paracentrotus lividus in the French Mediterranean there is no evidence of mass mortalities of Psammechinus miliaris associated with this disease around Britain and Ireland.

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

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

Targeted removal of characterizing species IR.LIR.KVS.Cod, IR.LIR.KVS.SlatPhyVS & IR.LIR.KVS.SlatPsaVS would likely have a fundamental effect on the character of the biotopes. Saccharina latissima is commercially cultivated, however typically sporophytes are matured on ropes (Handå et al., 2013) and not directly extracted from the seabed, as is the case with Laminaria hyperborea (see Christie et al., 1998).  As a consequence related literature on which to assess the “resistance” of Saccharina latissima to targeted harvesting is sparse. Similarly at the time of writing, no evidence could be found to suggest that Codium spp. was extracted for commercial or recreational l purposes.  Psammechinus miliaris is targeted as a potential aquaculture species. When fed a nutritious diet in culture, the gonad biomass rapidly proliferates which can then be marketed as urchin “roe” (Kelly et al., 1998; 2000). However, Kelly (2000) concluded that there was no viability in a Psammechinus miliaris commercial fishery because of the low gonad content of wild populations. While some extraction of Psammechinus miliaris may conceivably develop for roe-enhancement through feeding artificial or nutrient enriched diets (Dr Maeve Kelly pers comm. From Kelly, 2000), this is currently not in practice within the UK.

Sensitivity assessment.  None of the characterizing species are commercially extracted from the seabed. If extracted in the future resistance would need to be re-assessed. This pressure has been assessed as ‘Not Relevant’.

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

Direct, physical impacts from harvesting are assessed through the abrasion and penetration of the seabed pressures. The sensitivity assessment for this pressure considers any biological/ecological effects resulting from the removal of non-target species on this biotope.  Incidental removal of the key characterizing species and associated species would alter the character of the biotope. IR.LIR.KVS.Cod, IR.LIR.KVS.SlatPhyVS and IR.LIR.KVS.SlatPsaVS are characterized by a canopy of Saccharina lattisima. Saccharina lattisima provides a canopy under which a variety of red seaweeds grow, includingPhyllophora sp. (as in IR.LIR.KVS.SlatPhyVS).The loss of the canopy due to incidental removal as by-catch would, therefore, alter the character of the habitat and result in the loss of species richness. The ecological services such as primary and secondary production provided by these species would also be lost. Codium spp. is also a key/characterizing species that may be removed through incidental/accidental by-catch. Removal Codium spp. would by definition also change biotope structure

Psammechinus miliaris may suffer as a result of trawling or dredging for other benthic species. Species with fragile tests such as urchins have been reported to be particularly sensitive to damage from mobile fishing gear (see Jennings & Kaiser, 1998; Bergman & van Santbrink, 2000). Kaiser & Spencer (1994) reported a ca 20 – 50% mortality in Psammechinus miliaris as a result of a single pass of an experimental 4 m beam trawl.

Sensitivity assessment. For this assessment, it has been assumed that incidental removal would result in complete removal of the characterizing species. Resistance has been assessed as Low resilience as High and sensitivity as Low.

Bibliography

  1. Airoldi, L., 2003. The effects of sedimentation on rocky coast assemblages. Oceanography and Marine Biology: An Annual Review, 41,161-236

  2. Allain, J-Y. 1978. Age et croissance de Paracentrotus lividus (Lamarck) et de Psammechinus miliaris (Gmelin) des côtes nord de Bretagne (Echinoidea). Cahiers de Biologie Marine, 19, 11-21.

  3. Andersen, G.S., Steen, H., Christie, H., Fredriksen, S. & Moy, F.E., 2011. Seasonal patterns of sporophyte growth, fertility, fouling, and mortality of Saccharina latissima in Skagerrak, Norway: implications for forest recovery. Journal of Marine Biology, 2011, Article ID 690375, 8 pages.

  4. Bégin, C. & Scheibling, R.E., 2003. Growth and survival of the invasive green alga Codium fragile ssp. tomentosoides in tide pools on a rocky shore in Nova Scotia. Botanica Marina, 46 (5), 404-412.

  5. Bekkby, T. & Moy, F.E., 2011. Developing spatial models of sugar kelp (Saccharina latissima) potential distribution under natural conditions and areas of its disappearance in Skagerrak. Estuarine Coastal and Shelf Science, 95 (4), 477-483.

  6. Bergman, M.J.N. & Van Santbrink, J.W., 2000b. Fishing mortality of populations of megafauna in sandy sediments. In The effects of fishing on non-target species and habitats (ed. M.J. Kaiser & S.J de Groot), 49-68. Oxford: Blackwell Science.

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

  8. Birkett, D.A., Maggs, C.A. & Dring, M.J., 1998a. Maerl. an overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Natura 2000 report prepared by Scottish Association of Marine Science (SAMS) for the UK Marine SACs Project., Scottish Association for Marine Science. (UK Marine SACs Project, vol V.). Available from: http://www.ukmarinesac.org.uk/publications.htm

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

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

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

  12. Bulleri, F. & Airoldi, L., 2005. Artificial marine structures facilitate the spread of a non‐indigenous green alga, Codium fragile ssp. tomentosoides, in the north Adriatic Sea. Journal of Applied Ecology, 42 (6), 1063-1072.

  13. Bunker, F., Maggs, C., Brodie, J. & Bunker, A., 2012. Seasearch Guide to Seaweeds of Britain and Ireland. Marine Conservation Society, Ross-on-Wye.

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

  15. Cabioch, L., Dauvin, J.C. & Gentil, F., 1978. Preliminary observations on pollution of the sea bed and disturbance of sub-littoral communities in northern Brittany by oil from the Amoco Cadiz. Marine Pollution Bulletin, 9, 303-307.

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

  17. Churchill, A.C. & Moeller, H.W., 1972. Seasonal patterns of reproduction in New York populations of Codium fragile (Sur.) Hariot Subsp. tomentosoides (van Goor) Silva. Journal of Phycology, 8 (2), 147-152.

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

  19. Connor, D.W., Allen, J.H., Golding, N., Howell, K.L., Lieberknecht, L.M., Northen, K.O. & Reker, J.B., 2004. The Marine Habitat Classification for Britain and Ireland. Version 04.05. Joint Nature Conservation Committee, Peterborough. www.jncc.gov.uk/MarineHabitatClassification.

  20. Conolly N.J. & Drew, E.A., 1985. Physiology of Laminaria. III. Effect of a coastal eutrophication on seasonal patterns of growth and tissue composition in Laminaria digitata and L. saccharina. Marine Ecology, Pubblicazioni della Stazione Zoologica di Napoli I, 6, 181-195.

  21. Cullinane, J.P., McCarthy, P. & Fletcher, A., 1975. The effect of oil pollution in Bantry Bay. Marine Pollution Bulletin, 6, 173-176.

  22. Daan, R. & Mulder, M., 1996. On the short-term and long-term impact of drilling activities in the Dutch sector of the North Sea ICES Journal of Marine Science, 53, 1036-1044.

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

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

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

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

  27. Dudgeon, S.R. & Johnson, A.S., 1992. Thick vs. thin: thallus morphology and tissue mechanics influence differential drag and dislodgement of two co-dominant seaweeds . Journal of Experimental Marine Biology and Ecology, 165, 23-43.

  28. Elmhirst, R., 1922. Notes on the breeding and growth of marine animals in the Clyde Sea area. Report of the Scottish Marine Biological Association, 19-43.

  29. Farell, P. & Fletcher, R., 2000. The biology and distribution of the kelp, Undaria pinnatifida (Harvey) Suringar, in the Solent. In Solent Science - A Review (ed. M. Collins and K. Ansell), pp. 311-314. Amsterdam: Elsevier Science B.V.

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

  31. Fletcher, R.L. & Manfredi, C., 1995. The occurrence of Undaria pinnatifida (Phyaeophyceae, Laminariales) on the South Coast of England. Botanica Marina, 38 (4), 355-358.

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

  33. Fralick, R.A. & Mathieson, A.C., 1972. Winter fragmentation of Codium fragile (Suringar) Hariot ssp. tomentosoides (van Goor) Silva (Chlorophyceae, Siphonales) in New England. Phycologia, 11 (1), 67-70.

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

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

  36. Gantt, E., 1990. Pigmentation and photoacclimation. In Biology of the Red Algae (ed. K.M. Cole and R.G. Sheath), 203-219. Cambridge University Press.

  37. Gerard, V.A. & Du Bois, K.R., 1988. Temperature ecotypes near the southern boundary of the kelp Laminaria saccharina. Marine Biology, 97, 575-580.

  38. Gerard, V.A. & Mann, K.H., 1979. Growth and production of Laminaria longicruris ( Phaeophyta) populations exposed to different intensities of water movement 1. Journal of Phycology, 15 (1), 33-41.

  39. Gezelius, G., 1962. Adaptation of the sea urchin Psammechinus miliaris to different salinities. Zoologiska Bidrag fran Uppsala, 35, 329-337.

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

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

  42. Griffiths, A.B., Dennis, R. & Potts, G.W., 1979. Mortality associated with a phytoplankton bloom off Penzance in Mount's Bay. Journal of the Marine Biological Association of the United Kingdom, 59, 515-528.

  43. Handå, A., Forbord, S., Wang, X., Broch, O.J., Dahle, S.W., Storseth, T.R., Reitan, K.I., Olsen, Y. & Skjermo, J., 2013. Seasonal and depth-dependent growth of cultivated kelp (Saccharina latissima) in close proximity to salmon (Salmo salar) aquaculture in Norway. Aquaculture, 414, 191-201.

  44. Hanisak M.D., 1979. Effect of indole-3-acetic acid on growth of Codium fragile subsp tomentosoides (Chlorophyceae) in culture. Journal of Phycology 15, 124-127.

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

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

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

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

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

  50. Jackson, A., 2008. Ciona intestinalis. A sea squirt. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [On-line]. Plymouth: Marine Biological Association of the United Kingdom. [cited 16/12/15] Available from: http://www.marlin.ac.uk/species/detail/1369

  51. Jennings, S. & Kaiser, M.J., 1998. The effects of fishing on marine ecosystems. Advances in Marine Biology, 34, 201-352.

  52. Johansson, P., 2009. Effects of intermittent exposure of marine pollutants on sugar kelp and periphyton. Department of Plant and Environmental Sciences, University of Gothenburg.

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

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

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

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

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

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

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

  60. Kaiser, M.J., & Spencer, B.E., 1994a. A preliminary assessment of the immediate effects of beam trawling on a benthic community in the Irish Sea. In Environmental impact of bottom gears on benthic fauna in relation to natural resources management and protection of the North Sea. (ed. S.J. de Groot & H.J. Lindeboom). NIOZ-Rapport, 11, 87-94.

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

  62. Kelly, M.S., 2000. The reproductive cycle of the sea urchin Psammechinus miliaris (Echinodermata: Echinoidea) in a Scottish sea loch. Journal of the Marine Biological Association of the United Kingdom, 80, 909-919.

  63. Kelly, M.S., 2001. Environmental parameters controlling gametogenesis in the echinoid Psammechinus miliaris. Journal of Experimental Marine Biology and Ecology, 266, 67-80.

  64. Kelly, M.S., Brodie, C.C., & McKenzie, J.D., 1998. Somatic and gonadal growth of the sea urchin Psammechinus miliaris (Gmelin) maintained in polyculture with the Atlantic salmon. Journal of Shellfish Research, 17, 1557-1562.

  65. Kelly, M.S., Hunter, A.J., Scholfield, C. & McKenzie, J.D., 2000. Morphology and survivorship of larval Psammechinus miliaris in response to varying food conditions. Aquaculture, 183, 233-240.

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

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

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

  69. Lüning, K., 1979. Growth strategy of three Laminaria species (Phaeophyceae) inhabiting different depth zones in the sublittoral region of Hegloland (North Sea). Marine Ecological Progress Series, 1, 195-207.

  70. Lein, T.E, Sjotun, K. & Wakili, S., 1991. Mass - occurrence of a brown filamentous endophyte in the lamina of the kelp Laminaria hyperborea (Gunnerus) Foslie along the south western coast of Norway Sarsia, 76, 187-193.

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

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

  73. Lindahl, P.E. & Runnström, J., 1929. Variation und Ökologie von Psammechinus miliaris (Gmelin). Acta Zoologica, 10, 401-484.

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

  75. Maes, P., Jangoux, M., & Fenaux, L., 1986. La maladie de l''oursin-chauve': Ultrastructure des lésions et charactérisation de leur pigmentation. Annales de l'Institut Océanographique. Nouvelle série, 62, 37-45.

  76. MarLIN, 2015. MarLIN (Marine Life Network). (13-10-2015). http://www.marlin.ac.uk

  77. Mathieson, A.C. & Burns, R.L., 1975. Ecological studies of economic red algae. 5. Growth and reproduction of natural and harvested populations of Chondrus crispus Stackhouse in New Hampshire. Journal of Experimental Marine Biology and Ecology, 17, 137-156.

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

  79. Molenaar, F.J. & Breeman, A.M., 1994. Ecotypic variation in Phyllophora pseudoceranoides (Rhodophyta) ensures winter reproduction throughout its geographic range. Journal of Phycology, 30 (3), 392-402.

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

  81. Mortensen, T.H., 1927. Handbook of the echinoderms of the British Isles. London: Humphrey Milford, Oxford University Press.

  82. Moy, F., Alve, E., Bogen, J., Christie, H., Green, N., Helland, A., Steen, H., Skarbøvik, E. & Stålnacke, P., 2006. Sugar Kelp Project: Status Report No 1. SFT Report TA-2193/2006, NIVA Report 5265 (in Norwegian, with English Abstract), 36 pp.

  83. Moy, F.E. & Christie, H., 2012. Large-scale shift from sugar kelp (Saccharina latissima) to ephemeral algae along the south and west coast of Norway. Marine Biology Research, 8 (4), 309-321.

  84. Newroth, P.R., 1972. Studies on life histories in the Phyllophoraceae. II. Phyllophora pseudoceranoides and notes on P. crispa and P. heredia (Rhodophyta, Gigartinales). Phycologia, 11 (2), 99-107.

  85. Newton, L.C. & McKenzie, J.D., 1995. Echinoderms and oil pollution: a potential stress assay using bacterial symbionts. Marine Pollution Bulletin, 31, 453-456.

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

  87. Norton, T.A., 1978. The factors influencing the distribution of Saccorhiza polyschides in the region of Lough Ine. Journal of the Marine Biological Association of the United Kingdom, 58, 527-536.

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

  89. Parke, M., 1948. Studies on British Laminariaceae. I. Growth in Laminaria saccharina (L.) Lamour. Journal of the Marine Biological Association of the United Kingdom, 27, 651-709.

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

  91. Peteiro, C. & Freire, O., 2013. Biomass yield and morphological features of the seaweed Saccharina latissima cultivated at two different sites in a coastal bay in the Atlantic coast of Spain. Journal of Applied Phycology, 25(1), 205-213.

  92. Peters, A.F. & Schaffelke, B., 1996. Streblonema (Ectocarpales, Phaeophyceae) infection in the kelp Laminaria saccharina in the western Baltic. Hydrobiologia, 326/327, 111-116.

  93. Pizzolla P.F., 2007. Codium tomentosum Velvet horn. 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 10.02.16]. Available from: http://www.marlin.ac.uk/species/detail/1474

  94. Provan, J., Murphy, S. & Maggs, C.A., 2005. Tracking the invasive history of the green alga Codium fragile ssp. tomentosoides. Molecular Ecology, 14, 189-194.

  95. Ramus, J., Beale, S.I. & Mauzerall, D., 1976. Correlation of changes in pigment content with photosynthetic capacity of seaweeds as a function of water depth. Marine Biology, 37 (3), 231-238.

  96. Read, P.A., Anderson, K.J., Matthews, J.E., Watson, P.G., Halliday, M.C. & Shiells, G.M., 1983. Effects of pollution on the benthos of the Firth of Forth. Marine Pollution Bulletin, 14, 12-16.

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

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

  99. Schäfer, S. & Köhler, A., 2009. Gonadal lesions of female sea urchin (Psammechinus miliaris) after exposure to the polycyclic aromatic hydrocarbon phenanthrene. Marine environmental research, 68 (3), 128-136.

  100. SeaTemperature, 2015. World Sea Temperatures. (15/10/2015). http://www.seatemperature.org/

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

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

  103. Sjøtun, K. & Fredriksen, S., 1995. Growth allocation in Laminaria hyperborea (Laminariales, Phaeophyceae) in relation to age and wave exposure. Marine Ecology Progress Series, 126, 213-222.

  104. Sjøtun, K., 1993. Seasonal lamina growth in two age groups of Laminaria saccharina (L.) Lamour. in Western Norway. Botanica Marina, 36, 433-441.

  105. Sjøtun, K., Fredriksen, S. & Rueness, J., 1998. Effect of canopy biomass and wave exposure on growth in Laminaria hyperborea (Laminariaceae: Phaeophyta). European Journal of Phycology, 33, 337-343.

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

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

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

  109. Spicer, J.I., 1995. Oxygen and acid-base status of the sea urchin Psammechinus miliaris during environmental hypoxia. Marine Biology, 124, 71-76.

  110. Staehr, P.A. & Wernberg, T., 2009. Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. Journal of Phycology, 45, 91-99.

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

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

  113. Suchanek, T.H., 1993. Oil impacts on marine invertebrate populations and communities. American Zoologist, 33, 510-523.

  114. Svendsen, P., 1972. Some observations on commercial harvesting and regrowth of Laminaria hyperborea. Fisken og Havet, 2, 33-45.

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

  116. Thomsen, M. & McGlathery, K., 2006. Effects of accumulations of sediments and drift algae on recruitment of sessile organisms associated with oyster reefs. Journal of Experimental Marine Biology and Ecology, 328 (1), 22-34.

  117. Thomsen, M.S. & McGlathery, K.J., 2007. Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biological Invasions, 9 (5), 499-513.

  118. Trowbridge, C.D., 1995. Establishment of the green alga Codium fragile ssp. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. Journal of Ecology, 83 (6), 949-965.

  119. Trowbridge, C.D., 1996. Introduced versus native subspecies of Codium fragile: how distinctive is the invasive subspecies tomentosoides? Marine Biology, 126 (2), 193-204.

  120. Trowbridge, C.D., 1999. An assessment of the potential spread and options for control of the introduced green macroalga Codium fragile ssp. tomentosoides on Australian shores.  Commonwealth Scientific and Industrial Research Organisation. CRIMP Consultancy Report.

     

  121. Trowbridge, C.D., 1998. Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive or non-invasive subspecies. Oceanography and Marine Biology: an Annual Review, 36, 1-64.

  122. Ursin, E., 1960. A quantitative investigation of the echinoderm fauna of the central North Sea. Meddelelser fra Danmark Fiskeri-og-Havundersogelser, 2 (24), pp. 204.

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

Citation

This review can be cited as:

Stamp, T.E., 2015. [Saccharina latissima] with [Phyllophora] spp. and filamentous green seaweeds on variable or reduced salinity 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. Available from: http://www.marlin.ac.uk/habitat/detail/184

Last Updated: 16/12/2015