Foliose red seaweeds on exposed lower infralittoral rock

30-05-2002
Researched byGeorgina Budd Refereed byThis information is not refereed.
EUNIS CodeA3.116 EUNIS NameFoliose red seaweeds on exposed lower infralittoral rock

Summary

UK and Ireland classification

EUNIS 2008A3.116Foliose red seaweeds on exposed lower infralittoral rock
EUNIS 2006A3.116Foliose red seaweeds on exposed lower infralittoral rock
JNCC 2004IR.HIR.KFaR.FoRFoliose red seaweeds on exposed lower infralittoral rock
1997 BiotopeIR.EIR.KFaR.FoRFoliose red seaweeds on exposed or moderately exposed lower infralittoral rock

Description

A dense turf of foliose red seaweeds (including Plocamium cartilagineum, Cryptopleura ramosa and Delesseria sanguinea) on exposed or moderately exposed lower infralittoral rock, generally at or below the lower limit of the kelp. Most of the red seaweeds are common to the kelp zone above, while the faunal component of the biotope is made up of species that are found either in the kelp zone or the animal-dominated upper circalittoral below. The red seaweed species composition varies considerably and at some sites a single species may dominate (particularly Plocamium cartilagineum or Cryptopleura ramosa) As well as a varied red seaweed component, this biotope may also contain occasional kelp plants and patches of the brown foliose seaweed Dictyota dichotoma. In some areas Dictyota dichotoma may occur at high densities (see EIR.FoR.Dic). Other red seaweed-dominated biotopes occur in less wave-exposed areas (MIR.PolAhn), though they are affected by sand scour and are characterized by seaweeds that are resilient to the scouring. (Information taken from the Marine Biotope Classification for Britain and Ireland, Version 97.06: Connor et al., 1997a, b).

Recorded distribution in Britain and Ireland

Present on most coasts of the British Isles with areas where it is not recorded or known to be present from the south east coast of Britain and the east coast of Ireland.

Depth range

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Habitat review

Ecology

Ecological and functional relationships

Foliose algae provide shelter for invertebrates, a substratum for attachment of some species and food for grazers. Dependant relationships develop and are noted below.
  • The predominant environmental factor determining occurrence of this biotope is light. In the lower infralittoral there is generally insufficient light for the growth of Laminariales and substratum is dominated by foliose and encrusting red algae.
  • Old stipes and midribs of Delesseria sanguinea become heavily encrusted with algae and epiphytic invertebrates such as bryozoa, sponges and ascidians (Maggs & Hommersand, 1993).
  • The most important grazer of subtidal algae in the British Isles is the sea urchin, Echinus esculentus. It has demonstrated a preference for red algae. Sea urchin grazing may maintain the patchy and species rich understorey epiflora/fauna by preventing dominant species from becoming established. In wave exposed situations, sea urchins may not be able to cling on or feed in shallow depths during storms and this may favour the development of algal dominated biotopes. Also sea urchin densities vary in different parts of the coast, where numbers are low the biotope may be favoured (K. Hiscock, pers. comm.). Vost (1983) examined the effect of removing grazing Echinus esculentus and found that after 6-10 months the patchiness of the understorey algae had decreased and the species richness and biomass of epilithic species increased. Algae with single attachment points became more frequent in the urchin free area and the total biomass and species richness of epilithic species increased (Birkett et al., 1998b). Echinus esculentus grazing probably controls the lower limit of kelp distribution in some locations, e.g. in the Isle of Man (Jones & Kain 1967; Kain et al. 1975; Kain 1979).
  • Echinus esculentus may be preyed upon by the lobster Homarus gammarus, and in the north, the wolf-fish Anarhichas lupus.
  • The prosobranch mollusc Lacuna parva grazes extensively upon the red algae Phyllophora crispa and Delesseria sanguinea and Phycodrys rubens. Phyllophora crispa is the main substratum for spawn deposition (Ockelmann & Nielsen, 1981).
  • Corallina officinalis may support epiphytes, including Mesophyllum lichenoides, Titanoderma pustulatum, and Titanoderma corallinae, the latter causing tissue damage (Irvine & Chamberlain 1994). Hay et al. (1987) suggested that grazing by amphipods and polychaetes caused damage to 1-20 % of the blade area of the foliose brown algae Dictyota dichotoma
  • Other grazers include topshells, e.g. Gibbula cineraria and small Crustacea (amphipods and isopods) and the painted top-shell Calliostoma zizyphinum, which feeds upon cnidarians, as well as micro-organisms and detritus.
  • Specialist predators of hydroids and bryozoans in particular include the nudibranch species such as Janolus cristatus, Doto spp. and Onchidoris spp. Starfish (e.g. Asterias rubens, Crossaster papposus and Henricia spp.) are generalist predators feeding on most epifauna, including ascidians.
  • Predation does not necessarily cause mortality. For instance, Metridium senile is attacked by Aeolidia papillosa and by Pycnogonum littorale. Alcyonium digitatum is attacked by the nudibranchTritonia hombergi and the mollusc Simnia patula, which also feeds upon the hydroid Tubularia indivisa.
  • Many inhabitants of the biotope are suspension feeders and are doubtless in competition for food, although moderately strong water movement and the relatively close proximity of the highly productive kelp forests of the upper infralittoral are likely to bring a plentiful supply of food. Ninety percent of kelp production is estimated to enter the detrital food webs of coastal areas, as particulate organic matter (POM) and dissolved organic matter (DOM), supporting biotopes beyond the kelp beds (Birkett et al., 1998b). Suspension feeders include barnacles, ascidians such as Clavelina lepadiformis and Aplidium punctum, and anthozoans such as Alcyonium digitatum, Urticina felina and Caryophyllia smithii and occasional sponge crusts. Larger prey items would be taken by Urticina felina and Metridium senile (Hartnoll, 1998).

Seasonal and longer term change

Many of the red seaweeds in this biotope have annual fronds, which typically die back in the autumn and regenerate in the spring. Consequently a seasonal change occurs in the seaweed cover, which is substantially reduced over the winter and becomes most dense between April to September. For example, the perennial Delesseria sanguinea exhibits a strong seasonal pattern of growth and reproduction. New blades appear in February and grow to full size by May -June becoming increasing battered or torn and the lamina are reduced to midribs by December (Maggs & Hommersand, 1993). Blade weight is maximal in midsummer, growth dropping in June and July and becoming zero in August (Kain, 1987). Several species of bryozoans and hydroids demonstrate seasonal cycles of growth in spring/summer and regression (die back) in late autumn/winter, over wintering as dormant stages or juvenile stages (see Ryland, 1976; Gili & Hughes, 1995; Hayward & Ryland, 1998). For example, the fronds of Bugula species are ephemeral, surviving about 3-4 months but producing two frond generations in summer before dying back in winter, although, the holdfasts are probably perennial (Eggleston, 1972a; Dyrynda & Ryland, 1982). The hydroid Tubularia indivisa that may occasionally occur in the biotope is an annual, dying back in winter (Fish & Fish, 1996), while the uprights of Nemertesia antennina die back after 4-5 months and exhibit three generations per year (spring, summer and winter) (see reviews; Hughes, 1977; Hayward & Ryland, 1998; Hartnoll, 1998). Many of the bryozoans and hydroid species are opportunists (e.g. Bugula flabellata) adapted to rapid growth and reproduction (r-selected), taking advantage of the spring/summer phytoplankton bloom and more favourable (less stormy) conditions (Dyrynda & Ryland, 1982; Gili & Hughes, 1995). Some species such as the ascidians Ciona intestinalis and Clavellina lepadiformis are effectively annual (Hartnoll, 1998). Therefore, the biotope is likely to demonstrate seasonal changes in the abundance or cover of both algae and fauna. Winter spawning species such as Alcyonium digitatum may take advantage of the available space for colonization.

Habitat structure and complexity

  • The biotope occurs over bedrock surfaces and large boulders, the nature of which provide a variety of surface aspects. The species composition probably varies with depth from the upper limit of the lower infralittoral towards the circalittoral. For example, foliose and encrusting red algae probably out compete the faunal turf species on tops of bedrock ridges, but decline on vertical surfaces and with depth.
  • The algal and faunal turf provides interstices and refuges for a variety of small organisms such as nemerteans, polychaetes, amphipods, and prosobranchs.
  • Larger mobile species include decapod crustaceans such as shrimps, crabs, hermit crabs, lobsters, sea urchins, starfish and fish. Such species are not highly faithful to the biotope, but probably utilize available rock ledges and crevices for shelter.

Productivity

Specific information concerning the biotope was not found. Foliose and encrusting red algae are primary producers in the EIR.FoR biotope, the biomass of which will enter the food chain indirectly in the form of detritus, algal spores and abraded algal particulates, or directly as food for grazing gastropods, sea urchins or fish. The biotope is likely, however, to receive more particulate and dissolved organic matter (POM & DOM) from kelp biotopes in the upper infralittoral. 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. Refer to EIR.LhypFa and EIR.LhyphR.

Recruitment processes

Recruitment into the biotope occurs as a result of spore or larval settlement and by migration. Information on some of the characterizing species is given below:
  • The onset of sexual reproduction in Delesseria sanguinea is stimulated by day length, Delesseria sanguinea is a short-day plant sensitive to a night-break (Kain, 1991; Kain, 1996]. Kain (1987) suggested that the southern limit of Delesseria sanguinea may be determined by winter temperatures. Studies in Roscoff and Helgoland support that observation; new blades formed in April - June at Roscoff, males plants in October - December, cystocarps and tetrasporangia in October - December, the last cystocarps found in April. Recruitment of Delesseria sanguinea occurred between February and April/June in both Roscoff and Helgoland (Molenaar & Breeman, 1997).
  • Corallina officinalis produces spores over a protracted period and can colonize artificial substratum within one week in the intertidal (Harlin & Lindbergh, 1977; Littler & Kauker, 1984).
  • Sea urchins most likely migrate into the biotope rather than settle directly there. However, maximum spawning of Echinus esculentus occurs in spring although individuals may spawn over a protracted period. Gonad weight is maximal in February / March in the English Channel (Comely & Ansell, 1989) but decreases during spawning in spring and then increases again through summer and winter until the next spawning; there is no resting phase. Spawning occurs just before the seasonal rise in temperature in temperate zones but is probably not triggered by rising temperature (Bishop, 1985). Planktonic development is complex and takes between 45 -60 days in captivity (MacBride, 1914). Recruitment is sporadic or variable depending on locality.
  • Hydroids are often the first organisms to colonize available space in settlement experiments (Gili & Hughes, 1995). For instance, Nemertesia antennina releases planulae on mucus threads, that increase potential dispersal to 5 -50m, depending on currents and turbulence (Hughes, 1977). Most species of hydroid in temperate waters grow rapidly and reproduce in spring and summer. Few species of hydroids have specific substratum requirements and many are generalists. Hydroids are also capable of asexual reproduction and many species produce dormant, resting stages, that are very resistant of environmental perturbation (Gili & Hughes, 1995).
  • Sponges may proliferate both asexually and sexually. A sponge can regenerate from a broken fragment, produce buds either internally or externally or release clusters of cells known as gemmules which develop into a new sponge. However, some sponges appear to be long-lived, slow growing and recruit infrequently. For instance, monitoring studies at Lundy revealed extremely slow growth and no recruitment of Axinella dissimilis (Hiscock, 1994).
  • Anthozoans, such as Alcyonium digitatum and Urticina felina are long lived with potentially highly dispersive pelagic larvae and are relatively widespread. They are not restricted to this biotope and would probably be able to recruit rapidly (refer to full MarLIN reviews). Similarly, Metridium senile has a long lived, dispersive planktonic planula larva. However, it is also capable of reproducing asexually by budding form the base, and colonizes space aggressively, forming clumps (Sebens, 1985; Hartnoll, 1998). Juveniles are susceptible to predation by sea urchins or overgrowth by ascidians (Sebens, 1985; 1986).
  • Development of Lacuna parva is direct and takes about two months at 10-11 °C . After copulation females may produce fertilized eggs for two to three months. The species has an annual life cycle with mating prior to the production of spawn between March and June, death of adults occurs throughout May and June, the main hatching of new recruits occurs in June and July (Ockelman & Nielsen, 1981).
  • Mobile fauna, crabs, fish and starfish, will probably recruit from the surrounding area either by migration or from planktonic larvae, as the community develops and food, niches and refuges become available, .

Time for community to reach maturity

It is likely that Rhodophyceae could recolonize an area from adjacent populations within a short period of time in ideal conditions but that recolonization from distant populations would probably take longer.

Many of the Rhodophyta e.g. Delesseria sanguinea, Plocamium cartilagineum, Dilsea carnosa and Corallina officinalis are perennial species that may persist for several years. For instance, Dickinson (1963) suggested a life span of 5-6 years for Delesseria sanguinea. However, Kain (1984) estimated that 1 in 20 specimens of Delesseria sanguinea may attain 9 - 16 years of age. Kain (1975) examined recolonization of cleared concrete blocks in a subtidal kelp forest. Red algae colonized blocks within 26 weeks in the shallow subtidal (0.8m) and 33 weeks at 4.4m. Delesseria sanguinea was noted within 41 weeks (8 months) at 4.4m in one group of blocks and within 56-59 days after block clearance in another group of blocks. This recolonization occurred during winter months following spore release and settlement, but not in subsequent samples (Kain, 1975). This suggests that colonization of Delesseria sanguinea in new areas is directly dependent on spore availability. 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.
Many of the sessile fauna present in the EIR.FoR biotope such as alcyonarians, ascidians and sponges, are present in the communities described by Sebens (1985) which were considered to be dynamic and fast growing. Smaller associated mobile species such as polychaetes and prosobranchs have planktonic larvae and would most likely colonize after a year. Large mobile species such as sea urchins, starfish and crabs would migrate into the area rapidly. The community may therefore take probably two or three years to reach maturity, but competitive interactions and the arrival of slower colonizing species could mean that dynamic stability is not achieved for several years.

Additional information

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Preferences & Distribution

Recorded distribution in Britain and IrelandPresent on most coasts of the British Isles with areas where it is not recorded or known to be present from the south east coast of Britain and the east coast of Ireland.

Habitat preferences

Depth Range
Water clarity preferences
Limiting Nutrients Nitrogen (nitrates)
Salinity
Physiographic
Biological Zone
Substratum
Tidal
Wave
Other preferences Wave exposure

Additional Information

  • Nitrogen is the primary resource that limits seaweed growth and consequently variations in seaweed growth should parallel variations in nitrogen supply (Lobban & Harrison, 1997).
  • in wave exposed situations the sea urchin, Echinus esculentus, may experience difficulty maintaining contact with the rock whilst grazing in shallow waters owing to turbulence caused by wave action. Such disturbance may favour the development of this algal dominated biotope.

Species composition

Species found especially in this biotope

    Rare or scarce species associated with this biotope

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    Additional information

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    Sensitivity reviewHow is sensitivity assessed?

    Explanation

    The biotope is dominated by foliose and encrusting red algae, such as Delesseria sanguinea, Plocamium cartilagineum, Cryptopleura ramosa, Phycodrys rubens, Dilsea carnosa, Heterosiphonia plumosa and Corallinaceae. Delesseria sanguinea has been selected as an important characterizing species representative of the foliose red algae, as it occurs with the highest percentage frequency (Connor et al., 1997a). Lithophyllum incrustans represents the encrusting Corallinaceae. The edible sea urchin, Echinus esculentus, has been assessed to be a key functional species within the EIR.FoR biotope. Its grazing activity may help maintain the patchy and species rich epiflora/fauna by preventing species from becoming dominant (see Vost, 1983). Other important species include representatives of the sessile epifauna; anemones, soft corals, hydroids, bryozoans, ascidians and grazing molluscs such as Calliostoma zizyphinum. Mobile species such as crabs and fish are not faithful to the biotope although their sensitivity will be integrated where appropriate.

    Species indicative of sensitivity

    Community ImportanceSpecies nameCommon Name
    Important otherAlcyonium digitatumDead man's fingers
    Important otherCalliostoma zizyphinumPainted top shell
    Important otherClavelina lepadiformisLight bulb sea squirt
    Important characterizingDelesseria sanguineaSea beech
    Important otherEchinus esculentusEdible sea urchin
    Important characterizingLithophyllum incrustansEncrusting coralline alga
    Important otherNemertesia antenninaSea beard
    Important otherUrticina felinaDahlia anemone

    Physical Pressures

     IntoleranceRecoverabilitySensitivitySpecies RichnessEvidence/Confidence
    High High Moderate Major decline High
    Removal of the substratum will result in removal of all the attached species, together with most of the slow mobile faunal species (Crustacea, sea urchins and starfish) and an intolerance of high has been recorded. Recoverability is likely to be high (see additional information below).
    Intermediate High Low Decline Moderate
    Species such as Balanus crenatus, Bugula turbinata and Clavelina lepadiformis were assessed to have a high intolerance to smothering, owing to a combination of small size (zooids of Clavelina lepadiformis typically only grow up to 2 cm in height), inhibition of respiration and prevention of feeding. Fronds of adult Delesseria sanguinea are up to 30cm in height and would survive smothering to a depth of 5cm by sediment. However, algal spores and propagules would be adversely affected by a layer of sediment, which can exclude up to 98 % of light (Vadas et al., 1992). Holme & Wilson (1985) suggested that Urticina felina would survive periodic smothering of up to 5cm of sand, by being able to extend its column to maintain its disc above the sand surface. Smothered Echinus esculentus are unlikely to be able to move through sediment. However, individuals are unlikely to starve within a month. Comely & Ansell (1988) recorded large Echinus esculentus from kelp beds on the west coast of Scotland in which the substratum was seasonally covered with "high levels" of silt. This suggests that Echinus esculentus is unlikely to be killed by smothering, however, smaller specimens and juveniles may be more intolerant. Intolerance has been assessed to be intermediate, whilst germlings of algal species may be killed, adult plants are likely to survive and are perennials, so would recruit the following year. Some populations of faunal species would be degraded. Recoverability has been assessed to be high (see additional information below).
    Intermediate High Low Decline Moderate
    Increased suspended sediment may increase sediment scour, especially in winter. Spores and germlings are likely to be highly intolerant of sediment scour (Vadas et al., 1992). Delesseria sanguinea reproduces in winter and increased siltation may interfere with recruitment and long term survival of the population. Significant sediment cover of the middle to lower intertidal in a South Californian shore, resulting from fresh water runoff, caused substantial decline in Corallina spp. cover (Seapy & Littler, 1982). Alcyonium digitatum has been shown to be tolerant of high levels of suspended sediment. Hill et al. (1997) demonstrated that Alcyonium digitatum sloughed off settled particles with a large amount of mucous. Bryozoans are suspension feeding organisms that may be adversely affected by increases in suspended sediment, due to clogging of their feeding apparatus. Similarly increased siltation may clog up the feeding apparatus of Nemertesia spp. requiring energetic expenditure to clear. Intolerance has been assessed to be intermediate as the viability of some faunal species may be affected and in the worst instance recruitment of an important characterizing red algae may be inhibited. On return to prior conditions recoverability has been assessed to be high (see additional information below).
    Low High Moderate Minor decline Low
    For a period of one month a decline in the amount of suspended sediment is unlikely to be significant to the biotope. Suspension feeders such as Alcyonium digitatum and Clavelina lepadiformis would suffer a reduced food supply and increased competition, but on return to prior conditions optimal feeding would probably resume rapidly. However, bryozoans turfs are often abundant in clear, fast flowing waters (Moore, 1977a). A decrease in suspended sediment is likely to increase the abundance of bryozoans, including species of Bugula, consequently species richness may increase. Intolerance has been assessed to be low.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    The biotope is sublittoral, desiccation would not be relevant.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    The biotope is sublittoral, changes in the emergence regime would not be relevant.
    Not sensitive* Not relevant
    The biotope is sublittoral, changes in the emergence regime would not be relevant.
    High High Moderate Decline Low
    Typically water flow rates are moderately strong. Increased water flow is likely to reduce the population of large sea urchins. Echinus esculentus was observed to be rolled along the substratum by currents of 2.6 knots or above (Comely & Ansell, 1988). A reduction in grazing by Echinus esculentus would reduce patchiness, possibly allowing fewer species to dominate the biotope (see Vost, 1983) Furthermore, the increased sediment scour (the biotope probably receives a considerable amount of particulate organic matter from the highly productive upper infralittoral kelp biotopes) likely to accompany increased water flow rates may be more damaging. Over the period of a year animal species such as Halichondria panicea, Balanus crenatus and Tubularia indivisa that flourish in fast flowing water are likely to out-compete the algae and become dominant, changing the biotope to a community more like ECR.BalHpan. Intolerance has been assessed to be high. On return to less strong water flows, fast settling algae would again dominate and the abundance of animals decline as natural mortality occurred. Therefore recoverability has been assessed to be high.
    Low High Low Rise Moderate
    Water movement is essential for suspension feeders such as hydroids, bryozoans, sponges, amphipods and ascidians to supply adequate food, remove metabolic waste products, prevent accumulation of sediment and disperse larvae or medusae. For instance a decreased water flow rate may impact upon Alcyonium digitatum in that feeding efficiency could decrease as less material (phytoplankton & zooplankton) would be brought into contact with the colonies. Also a lower energy environment favours siltation. However deep growing red algae such as Delesseria sanguinea were observed growing in stagnating water in Kiel Bay, western Baltic Sea (Schwenke, 1960, cited in Kinne, 1971). It is likely therefore that Delesseria sanguinea would be not sensitive to decreased water flow rate. Intolerance has been assessed to be low as the viability of some faunal species may be affected.
    Intermediate High Low Decline Low
    The tolerance of red algae to temperature changes varies considerably and those of the littoral zone typically have a greater tolerance to both increased and decreased temperature, than those of the sublittoral (see Gessner, 1970, for investigation of the effects of temperature on marine red algae). Sublittoral red algal species, Sphondylothamnion multifidum, Cryptopleura ramosa and Rhodophyllis divaricata were capable of surviving at 27 °C, while other species such as Callophyllis laciniata, Calliblepharis ciliata, Plocamium cartilagineum and Heterosiphonia plumosa died within 12 hours in seawater at 27 °C. However, such a temperature increase exceeds that of the benchmark level. Balanus crenatus is a boreal species, and is intolerant of increases in water temperature. In Queens Dock, Swansea where the water was on average 10 °C higher than average due to the effects of a condenser effluent, Balanus crenatus was replaced by the subtropical barnacle Balanus amphitrite. After the water temperature cooled Balanus crenatus returned (Naylor, 1965). Bishop (1985) noted that gametogenesis of Echinus esculentus proceeded at temperatures between 11 - 19 °C although continued exposure to 19 °C destroyed synchronicity of gametogenesis between individuals. Embryos and larvae developed abnormally after up to 24hr at 15 °C (Tyler & Young, 1998). Bishop (1985) suggested that Echinus esculentus could not tolerate high temperatures for prolonged periods due to increased respiration rate and resultant metabolic stress. Therefore, although Echinus esculentus would probably have a low intolerance to chronic long term temperature change it is likely to be more intolerant of sudden or short term acute change (e.g. 5 °C for 3 days) in temperature. The British Isles are near the southern limit of range of some species such as Lacuna vincta. Long term increases in temperature may limit the survival of the snail, restricting subsequent distribution. Short term acute temperature increases may cause death. However, other prosobranch species would replace Lacuna vincta, or other northern species, if lost from the biotope. Intolerance has been assessed to be intermediate as some species may be lost. Recoverability has been assessed to be high (see additional information below).
    Intermediate High Low Minor decline Low
    The tolerance of red algae to temperature change varies considerably and those of the littoral typically have a greater tolerance to both increased and decreased temperature, than those of the sublittoral. Cold damage usually changes the colour of red algae to a bright yellow orange. Sphondylothamnion multifidum, Cryptopleura ramosa and Rhodophyllis divaricata were partially or completely killed at 5 °C. Callophyllis laciniata, Calliblepharis ciliata, Plocamium cartilagineum and Heterosiphonia plumosa survived -2 °C. Delesseria sanguinea and Phycodrys rubens succumbed at temperatures of -3 °C to -5 °C. During experimental attempts to adapt red algae to cold by maintaining them at -1 °C to + 1 °C for several months, a drop in the lethal temperature tolerance of Delesseria sanguinea and a few other species was detected, in the order of 1 to 2 °C (Gessner, 1970). Although Urticina felina was apparently unaffected by the extremely cold winter of 1962/3 (Crisp, 1964), Gosse (1860) observed that "after the intense and protracted frost of February 1855, the shores of South Devon were strewn with dead and dying anemones, principally of this species". Bearing in mind the equivocal observations from two cold winters, it is suggested that at least some individuals might be killed by extreme cold. Alcyonium digitatum was also reported to be apparently unaffected by the severe winter of 1962-1963 (Crisp, 1964). Evidence suggests that some species (both faunal and floral) would be adversely affected by an acute temperature decrease and intolerance has been assessed to be intermediate. On return to prior conditions recovery is likely and has been assessed to be high.
    Low Very high Very Low No change Low
    Increased turbidity would probably reduce the photosynthetic capability of the algae and reduce the food available for suspension feeders, as phytoplanktonic production is also likely to be inhibited over the period of one year. Intolerance has been assessed to be low as effects of increased turbidity would probably be most significant at the sub lethal level. On return to prior conditions recovery is likely to be rapid.
    High High Intermediate Rise Low
    A decrease in turbidity may increase phytoplankton and hence zooplankton productivity and potentially increase food availability. However, increased light penetration may favour the development of a kelp canopy which would change the biotope to one characterized by kelp species. Although the majority of the community would survive as an understorey fauna in the presence of a kelp canopy an intolerance of high has been recorded, as the EIR.FoR biotope may not be recognized. However, if rock is present deeper than the biotope, a decrease in turbidity may allow the biotope to extend downwards, thus shifting the depth band in which the biotope occurs. On return to prior conditions recoverability has been assessed to be high as species would remain in the biotope.
    Low High Low Minor decline Low
    The biotope typically occurs in situations that are very exposed to moderately exposed and, at the depth where the biotope occurs, wave action is likely to be a significant environmental factor. For instance, red algae which are characteristic of the biotope, are favoured in wave exposed sites. Delesseria sanguinea occurs on coasts with a wide range of wave exposures, from very exposed to very sheltered and are therefore is likely to be relatively tolerant of increased wave action. Of the animal species, Bugulaspp. produce flexible erect tufts, which are likely to move with the oscillatory flow created by wave action but Nemertesia spp. are intolerant of high wave exposure and so are only found in more sheltered areas. Whilst it might be expected that some important characterizing and key functional species such as Echinus esculentus are likely to be displaced or damaged by strong wave action and alterations in abundance occur, intolerance has been assessed to be low as the biotope would still be recognisable. Recoverability has been assessed to be high (see additional information below).
    Low High Low Rise Moderate
    The moderately strong to weak tidal currents typical of this biotope are probably more important for water movement than wave induced oscillatory flow. Therefore, a decrease in wave action may allow more delicate species, such as Nemertesia ramosa, ascidians and sponges to increase in abundance. Decreased wave action may allow the biotope to extend into shallower water. However, reduced wave action may result in an increase in sea urchin predation and hence increased patchiness and species richness (Sebens, 1985; Hartnoll, 1998), but excessive grazing may create an urchin barren, in which case the biotope would be lost. Overall, a decrease in wave action may not adversely affect the biotope while the moderately strong currents maintain adequate water flow, and although some species in the biotope may change, important characterizing species of the biotope will probably survive. Therefore, an intolerance of low has been recorded.
    Tolerant Not relevant Not relevant No change Moderate
    Species within the biotope are likely to be not sensitive to noise at the benchmark level.
    Tolerant Not relevant Not relevant No change Moderate
    Species within the biotope are likely to be not sensitive to the visual presence of objects as described in the benchmark.
    Intermediate High Low Minor decline Low
    The growth form of Delesseria sanguinea and other foliose red algae suggests that its lamina would probably be damaged by abrasion but not removed. However, a passing scallop dredge would probably tear off a large proportion of the macroalgae and remove any associated species with them. Mobile species, such as isopods would probably avoid damage. Similarly, individuals in crevices or overhangs would probably be unaffected. Bradshaw et al. (2000) suggested that fragile species such a urchins (e.g. Echinus esculentus), suffered badly from impact with a passing scallop dredge. Other sessile faunal species such as Clavelina lepadiformis have relatively delicate growth forms and are likely to be damaged or removed by a passing dredge. Intolerance has been assessed to be intermediate as populations of species may be partially destroyed but the biotope would still be recognized. Recoverability has been assessed to be high (see additional information below).
    High High Moderate Major decline Low
    Red algae are permanently attached to the substratum, as are many faunal species. If displaced re-attachment is not possible. Red algae characterize the biotope, in their absence the biotope would not be recognized and intolerance has been assessed to be high. If populations of important characterizing species remain in the vicinity of the denuded substratum recruitment is likely to occur and recoverability has been assessed to be high (see additional information below).

    Chemical Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    High Moderate Moderate Major decline Moderate
    O'Brien & Dixon (1976) report that red algae are effective indicators of detergent damage since they undergo colour changes when exposed to relatively low concentrations. Smith (1968) reported that 10 ppm of the oil dispersive detergent BP 1002 killed the majority of specimens in 24hrs in toxicity tests. However, the effects take several days to manifest; when killed the algae turn bright orange. Smith (1968) also demonstrated that 0.5 -1ppm of the detergent BP1002 resulted in developmental abnormalities in echinopluteus larvae of Echinus esculentus. Echinus esculentus populations in the vicinity of an oil terminal in La Coruna Bay, Spain, showed developmental abnormalities in the skeleton. Hoare & Hiscock (1974) reported that red algae (e.g. Lithothamnia spp., Corallina officinalis, Polyides rotundus, Dilsea carnosa, Rhodymenia palmata and Desmarestia aculeata), echinoderms, Polyzoa and amphipod crustaceans appeared to be particularly intolerant of the reduction in water quality associated with the effluent discharged (containing free halogens, HCL & H2SO4) from a bromine extraction works into Amlwch Bay, Anglesey. Red algal species and the urchin Echinus esculentus are likely to be affected by synthetic chemicals, so intolerance has been assessed to be high. Recoverability has been assessed to be moderate as populations may not remain in the immediate vicinity of the biotope so that recruits are not readily available.
    Heavy metal contamination
    Intermediate Moderate Moderate Decline Very low
    Uptake of heavy metals from solution by seaweed is influenced by factors such as light, algal nitrogen content, frond age, length of emersion, temperature, salinity, season of the year and presence of other pollutants in the surrounding water (see Lobban & Harrison, 1997) and consequently seaweeds may not accurately reflect metal concentrations in the surrounding water. The order of metal toxicity to algae varies with the algal species and the experimental conditions, but generally the order is Hg>Cu>Cd>Ag>Pb>Zn (Rice et al., 1973; Rai et al., 1981), however insufficient information was available to comment further on the particular intolerance of algal species within the biotope. Kinne (1984) reported developmental disturbances in Echinus esculentus exposed to waters containing 25 µg / l of copper (Cu) and reduced species viability would result in the long term as the species fail to successfully recruit. The information available is patchy but there would appear to be some intolerance of species within the biotope to heavy metals and intolerance has been reported to be intermediate. Recovery should be rapid as heavy metals would not be accumulated in the substratum (as occurs with sediments) and most species in the biotope either have planktonic propagules or are likely to migrate into the area.
    Hydrocarbon contamination
    Intermediate High Low Decline Moderate
    O'Brien & Dixon (1976) concluded that red algae were the most sensitive group of algae to hydrocarbon or dispersant contamination, possibly attributable to the susceptibility of the photosynthetic pigment phycoerythrin to chemical damage. Following a series of laboratory and field experiments Grandy (1984) reported Delesseria sanguinea, Cryptopleura ramosa, Phycodrys rubens and Plocamium cartilagineum to be sensitive to oil/dispersant mixtures; Cryptopleura ramosa and Plocamium cartilagineum were the most sensitive and Phycodrys rubens the least sensitive. In toxicity experiments, Smith (1968) found Delesseria sanguinea to be particularly intolerant of the oil dispersant BP 1002; 10 ppm of BP 1002 was lethal to the species. Heavy mortality of Delesseria sanguinea was also observed down to a depth of 12 m after the Torrey Canyon oil spill (Drew et al., 1967). However, experience during the Torrey Canyon oil spill seems to be exceptional. As after the Esso Bernicia spill in 1978 in the Sullom Voe and heavy use of dispersants on significant quantities of oil, practically no damage to shallow (< 5 m) red algae could be found in Martins Haven (K. Hiscock, pers. comm.). Following the Sea Empress oil spill the most dramatic effect on the seaweeds was the marked bleaching of the encrusting coralline algae Lithothamnion incrustans and Phymatolithon purpureum. Corallina officinalis, Chondrus crispus and Mastocarpus stellatus also showed signs of bleaching. The encrusting corallines, however, recovered quickly, suggesting that the damage had been restricted to the surface layers (Y. Chamberlain, pers. comm. to Crump et al., 1999). At the depth at which this biotope occurs, only in the most severe conditions would damage probably occur to the characterizing species, and intolerance has been assessed to be intermediate. Recoverability has been assessed to be high assuming deterioration of contaminants (see additional information below).
    Radionuclide contamination
    No information Not relevant No information Not relevant Not relevant
    Insufficient
    information
    Changes in nutrient levels
    Intermediate High Low Decline Low
    Delesseria sanguinea can grow new blades in darkness by drawing on reserves held in the frond midrib and stipe (Lüning, 1990), suggesting that nutrients are subject to 'luxury' accumulation in the winter months. Delesseria sanguinea is likely to tolerate low nutrient levels, during spring and summer. An increase in abundance of red algae, including Delesseria sanguinea, was associated with eutrophication in the Skagerrak area, Sweden, especially in areas with the most wave exposure or water exchange (Johansson et al., 1998). However, where eutrophication resulted in high siltation rates, the delicate foliose red algae such as Delesseria sanguinea were replaced by tougher, erect red algae (Johansson et al., 1998). Lundäve (1990) reported the effects of a serious plankton bloom of Chrysochromulina polyepis in May-June 1998 on rocky-subtidal communities of the Swedish west coast. A site at 4.5 m depth contained small populations of ascidians, sponges and echinoderms in addition to the more dominant red algae, including Delesseria sanguinea and Corallina officinalis. In addition to almost total mortality of the faunal population, the site also showed severe damage to several of the algal species, by early June plants of Delesseria sanguinea lost all pigmentation. Whilst moderate nutrient may be beneficial, e.g. addition of nutrients may encourage the growth of ephemeral and epiphytic algae and therefore increase the food available to sea-urchin populations, severe nutrient enrichment is likely to cause the loss of important characterizing species. At the benchmark level intolerance has been assessed to be intermediate. On return to prior to prior conditions, recoverability has been assessed to be moderate. Lundäve (1990) observed significant changes in the rocky-subtidal community composition after the phytoplankton bloom, regeneration of Delesseria sanguinea was not observed, so following more severe episodes of nutrient enrichment the biotope may not recover.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    The biotope occurs in locations of full salinity.
    Intermediate High Low Minor decline Low
    Gessner & Schramm (1971) give a summary of the effects of salinity changes on marine algae. Most sublittoral red algae cannot withstand salinities below 15 psu. Echinoderms are generally unable to tolerate low salinity (stenohaline) and possess no osmoregulatory organ (Boolootian, 1966). The distribution of, and the depth at which Alcyonium digitatum occurs suggest that it is unlikely to survive significant dilution. Clavelina lepadiformis is tolerant of a wide range of salinities; Fish & Fish (1996) found that the ascidian could tolerate salinities as low as 14 psu. Braber & Borghouts (1977) found that Urticina felina (as Tealia felina) penetrated to about the 11ppt Chlorinity (about 20psu) isohaline at mid tide during average water discharge in the Westerschelde estuary suggesting that, during high river flow, it would be tolerant of reduced salinity conditions. Intertidal and rock pool individuals will also be subject to variations in salinity because of precipitation on the shore; albeit for short periods on the lower shore. Therefore, the species seems to have a high tolerance to reduction in salinity but may have to retract tentacles and suffer reduced opportunity to feed. The community is likely to tolerate a decrease in one salinity category of the MNCR salinity scale for one year, although some faunal species may decline in abundance as a result of intolerance or migration. A reduction in grazing pressure by Echinus esculentus may allow some algal species to dominate the biotope and species richness may decline. However, the biotope would still be recognized despite being impoverished so intolerance has been assessed to be intermediate and recoverability high on return to prior conditions (see additional information below).
    High High Moderate Major decline Moderate
    The effects of deoxygenation in plants has been little studied. However, a study of the effects of anaerobiosis on some marine algae reported Delesseria sanguinea to be very intolerant of anaerobic conditions; at 15 °C death occurred within 24hrs and no recovery took place, some specimens however survived at 5 °C. (Hammer, 1972). Under hypoxic conditions echinoderms become less mobile and stop feeding. 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). Alcyonium digitatum mainly inhabits environments in which the oxygen concentration usually exceeds 5 ml per litre and respiration is aerobic. Assimilation of oxygen occurs simply by diffusion through the epidermis of exposed tissues and transport to tissues is facilitated by hydroplasmic flow and ciliary activity (Hickson, 1901). It is likely that Alcyonium digitatum would be highly intolerant of a period of hypoxia. Delesseria sanguinea is an important characterizing species in its absence the biotope would not be recognized. Death of Delesseria sanguinea was recorded within 24 hours (see above) so it unlikely to survive anoxic conditions for a period on one week, unless temperatures are very low. Furthermore, sessile faunal species would probably be lost and mobile species are likely to migrate to avoid adverse conditions, so species richness would decline. On return to prior conditions recoverability has been assessed to be high if populations of important characterizing species are in the vicinity of the denuded substratum (see additional information below).

    Biological Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    No information Not relevant No information Not relevant Not relevant
    In Rhodophyta, viruses have been identified by means of electron microscopy (Lee, 1971) and it is obvious that they are widespread. However, nothing is known of their effects on growth or reproduction in red algae and experimental transfer from an infected to an uninfected specimen has not been achieved (Dixon & Irvine, 1977). Echinus esculentus 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 (Bower, 1996). It is thought to be caused by the bacteria Vibrio anguillarum and Aeromonas salmonicida. Bald sea-urchin disease was recorded from Echinus esculentus on the Brittany Coast. However, no evidence of mass mortalities of Echinus esculentus associated with disease have been recorded in Britain and Ireland.
    No information Not relevant No information Not relevant Not relevant
    There are currently no known non-native species that occur in, and, might adversely affect this biotope.
    Intermediate High Low Decline Low
    The collection of Echinus esculentus for the curio trade was studied by Nichols (1984). He concluded that the majority of divers collected only large specimens that are seen quickly and often missed individuals covered by seaweed or under rocks, especially if small. As a result, a significant proportion of the population remains. He suggested that exploited populations should not be allowed to fall below 0.2 individuals per square metre. Echinus esculentus has been identified as a key functional species, owing to its grazing which may prevent dominance of the biotope by a few species (see Vost, 1983). Intolerance has been assessed to be intermediate and recovery high via migration from adjacent biotopes. We have no evidence for the indirect effects of extraction of other species on this biotope.
    Not relevant Not relevant Not relevant Not relevant Not relevant

    Additional information

    Recoverability
    Red algal species particularly characteristic of the biotope would be expected to recover quickly. For instance, Kain (1975) examined recolonization of cleared concrete blocks in a subtidal kelp forest. Red algae colonized blocks within 26 weeks in the shallow subtidal (0.8m) and 33 weeks at 4.4m. Delesseria sanguinea was noted within 41 weeks (8 months) at 4.4m in one group of blocks and within 56-59 days after block clearance in another group of blocks. This suggests that Delesseria sanguinea can recolonize areas, but recolonization would be directly dependent on occurrence of reproductive season and spore availability. Corallina officinalis settled on artificial substances within 1 week of placement in the intertidal in New England, during summer (Harlin & Lindbergh, 1977). New fronds of Corallina officinalis appeared on sterilised plots within six months and 10 %cover was reached with 12 months (Littler & Kauker, 1984). 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. It is likely that red algae could recolonize an area from adjacent populations within a short period of time in ideal conditions but that recolonization from distant populations would probably take longer. Sponge species, Alcyonium digitatum and ascidians are all known to colonize bare surfaces rapidly. A short larval life and large numbers of larvae produced probably results in good local but poor long-range dispersal for bryozoans. Species of Bugula are opportunistic, capable of colonizing most hard substrata, and will probably colonize quickly in the vicinity of reproductive colonies, especially in the summer months in temperate waters. Once established, population abundance will probably also increase rapidly. Where the erect parts of colonies have been removed, regrowth from stolons may occur, resulting in rapid recovery. Therefore, bryozoan populations reduced in extent or abundance will probably recover within between 6 to 12 months in most cases due to local recruitment. Recoverability is likely to be slow in populations of Urticina felina where nearby individuals do not exist. The large size, slow growth rate and evidence from aquarium populations suggests that Urticina felina is long lived. Although it probably breeds each year there is no information regarding fecundity. Breeding probably does not occur until the anemone is at least 1.5 years old. Dispersal ability is considered to be poor in the similar Urticina eques (Solé-Cava et al., 1994). The larva is most likely benthic and, although unlikely to settle for many days after release (based on work on the similar Tealia crassicornis for north-west USA), is unlikely to travel far. However, assuming that there are populations surviving nearby recruitment is likely to occur over the short distances involved but how rapidly is uncertain. The mollusc Lacuna vincta has an annual life cycle, is highly fecund and its long planktonic larval stage means that successful recruitment from other populations is likely. Recovery of important characterizing red algal species is likely within 1-2 years and qualitative recovery of faunal species is probable within five years assuming that populations that may provide recruits are in the vicinity. Some long-lived slow growing species that recruit infrequently, such as the sponge Axinella dissimilis (Hiscock, 1994) may not return for many decades if lost. However, because the biotope would be recognized within a very few years, recoverability has been assessed to be high.

    Importance review

    Policy/Legislation

    Habitats Directive Annex 1Reefs

    Exploitation

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    Additional information

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    Citation

    This review can be cited as:

    Budd, G.C. 2002. Foliose red seaweeds on exposed lower 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/65

    Last Updated: 30/05/2002