Hydroids, ephemeral seaweeds and Littorina littorea in shallow eulittoral mixed substrata pools

Researched byCharlotte Marshall Refereed byThis information is not refereed.
EUNIS CodeA1.414 EUNIS NameHydroids, ephemeral seaweeds and Littorina littorea in shallow eulittoral mixed substrata pools

Summary

UK and Ireland classification

EUNIS 2008A1.414Hydroids, ephemeral seaweeds and Littorina littorea in shallow eulittoral mixed substrata pools
EUNIS 2006A1.414Hydroids, ephemeral seaweeds and Littorina littorea in shallow eulittoral mixed substrata pools
JNCC 2004LR.FLR.Rkp.HHydroids, ephemeral seaweeds and Littorina littorea in shallow eulittoral mixed substrata pools
1997 BiotopeLR.LR.Rkp.HHydroids, ephemeral seaweeds and Littorina littorea in shallow eulittoral mixed substrata pools

Description

Shallow pools on mixed cobbles, pebbles, gravel and sand may be colonized by hydroids (Obelia longissima and Kirchenpaueria pinnata), ephemeral green algae (Ulva sp.) and the winkle Littorina littorea. Within these pools, patches of sand may be occupied by the lugworm Arenicola marina and sand mason worms Lanice conchilega. These pools are often associated with mussel beds (SLR.MytX), with Mytilus edulis also present in the pools. Barnacles (Semibalanus balanoides and Elminius modestus) and the keel worm Pomatoceros triqueter may be attached to shells and small stones. (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

LR.H has not been recorded in Ireland. In Scotland, it has only been recorded at Devil's Thrashing Floor, Dumfries & Galloway. On the south Devon coast it is found near Brixham. On the west coasts it has been recorded near Port Talbot in Wales and at Duddon Sands and St Bees Head in Cumbria. It has also been recorded on the north coast of Norfolk and near Blackwater Estuary in Essex.

Depth range

Mid shore

Additional information

-

Listed By

Further information sources

Search on:

JNCC

Habitat review

Ecology

Ecological and functional relationships

This biotope is dominated by species able to withstand the frequent disturbance caused by wave action. The fact that LR.H rockpools are shallow and have a mixed substratum means that sand and pebbles will be frequently moved around the rockpool. This is especially true in stormy weather when larger cobbles and boulders may be moved into the pool and when the pool may be flushed clean of sediment. This in itself means that the community is unlikely to be a climax community, but more a transient community dominated by ephemeral, rapidly growing species that are able quickly to dominate space created by wave energy. Furthermore, both the flora and fauna are likely to vary both spatially, i.e. between rock pools, and on a temporal basis, depending on the frequency, severity and timing of disturbance.
  • Primary producers in this biotope are represented by ephemeral green algae such as Ulva sp. Ulva intestinalis can grow rapidly and is tolerant of a range of temperatures and salinities. Ulva intestinalis is also the preferred food of Littorina littorea (see below).
  • In terms of characterizing species, suspension feeders are the dominant trophic group in LR.H. The most common suspension feeders likely to be found in LR.H are the hydroid Obelia longissima and the common mussel Mytilus edulis. The acorn barnacle Semibalanus balanoides may also be common. Semibalanus balanoides actively feeds on detritus and zooplankton. Mytilus edulis actively feeds on bacteria, phytoplankton, detritus, and dissolved organic matter (DOM). Obelia longissima is a passive suspension feeder, feeding on small zooplankton, small crustaceans, oligochaetes, insect larvae and probably detritus. The branches of Obelia longissima may be used as substratum by Mytilus edulis pediveligers (Brault & Bourget, 1985). Other suspension feeders may include the barnacle Elminius modestus and the tubeworm Pomatoceros triqueter.
  • The grazing gastropod Littorina littorea feeds on range of fine red, green and brown algae including Ulva sp., Cladophora sp. and Ectocarpus sp.
  • Deposit feeding worms such as the sand mason Lanice conchilega and the lugworm Arenicola marina may be found if patches of sand are present in the pools. The sand mason is also capable of active suspension feeding.
  • The common shore crab Carcinus maenas is the largest mobile predator frequently associated with LR.H. Carcinus maenas is likely to move in and out of the rockpool feeding on plant and animal material including Semibalanus balanoides and Littorina littorea.

Seasonal and longer term change

Rockpools constitute a distinct environment for which physiological adaptations by the flora and fauna may be required (Lewis, 1964). Conditions within rockpools are the consequence of prolonged separation from the main body of the sea, and physico-chemical factors within them fluctuate dramatically (Huggett & Griffiths, 1986). Shallow pools such as those associated with LR.H are especially influenced by insolation, air temperature and rainfall, the effects of which become more significant towards the high shore, where pools may be isolated from the sea for a number of days or weeks (Lewis, 1964).

Water temperature in pools follows the temperature of the air more closely than that of the sea. In summer, shallow pools are warmer by day, but may be colder at night, and in winter may be much colder than the sea (Pyefinch, 1943). It is also possible that shallow pools may freeze over in the coldest winter months.

High air temperatures cause surface evaporation of water from pools, so that salinity steadily increases, especially in pools not flooded by the tide for several days. Alternatively, high rainfall will reduce pool salinity or create a surface layer of brackish/nearly fresh water for a period. The extent of temperature and salinity change is affected by the frequency and time of day at which tidal inundation occurs. If high tide occurs in early morning and evening the diurnal temperature follows that of the air, whilst high water at midday suddenly returns the temperature to that of the sea (Pyefinch, 1943). Heavy rainfall, followed by tidal inundation can cause dramatic fluctuations in salinity, and values ranging from 5-30 psu have been recorded in rockpools over a period of 24 hrs (Ranade, 1957). Rockpools in the supralittoral, littoral fringe and upper eulittoral are liable to gradually changing salinities followed by days of fully marine or fluctuating salinity at times of spring tide (Lewis, 1964).

Due to the frequent disturbances likely to affect this biotope, any seasonal changes are likely to be masked by changes caused by wave energy. Some species of 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 (Gili & Hughes, 1995). Many hydroids are opportunists adapted to rapid growth and reproduction (r-selected), taking advantage of the spring/summer phytoplankton bloom and more favourable (less stormy) conditions (Gili & Hughes, 1995). Brault & Bourget (1985) noted that Obelia longissima exhibited an annual cycle of biomass, measured as colony length, on settlement plates in the St Lawrence estuary. Colony length increased from settlement in June, reaching a maximum in November to March and then decreasing again until June, although the decline late in the year was attributed to predation, and data was only collected over a two year period. The ephemeral algae are also likely to experience an obvious decline in biomass over the winter months.

Habitat structure and complexity

The mixed substratum of the rockpool will give the habitat some heterogeneity since there is likely to be a mixture of sand, gravel, pebbles and cobbles. It is the surfaces of the larger pebbles and cobbles that are likely to be colonized by the algae, barnacles and tubeworms and hydroids although Obelia longissima can also grow on coarse clean sand. Clumps of mussels, whether the shells are empty or not, will also provide a substratum for the hydroids and barnacles. The mussel matrix will bind sediment and the sediment trapped between the shells may provide shelter for cryptic species and small worms, for example.

Productivity

No information was found regarding the productivity in LR.H although it is expected to be low. At any given time it is unlikely that there will be a well established community, regardless of species composition.

Recruitment processes

  • Obelia longissima exhibits a typical leptolid life cycle consisting of a sessile colonial, vegetative hydroid stage, a free-living sexual medusoid stage, and a planula larval stage (see MarLIN review). In terms of reproduction and recruitment, Obelia longissima has a number of strategies.
    • Obelia longissima can grow vegetatively and branch to form a network across the substratum. It can also reproduce by fission or mechanical fragmentation of the colony which may aid dispersal (Gili & Hughes, 1995). Hydroids can also form frustules or gemmules, which are thought to be resting stages, in response to stress (Gili & Hughes, 1995). These frustules are adhesive and stick to the substratum where they can form new colonies (Cornelius, 1995a; Kosevich & Marfenin, 1986).
    • In terms of sexual reproduction, Obelia longissima is dioecious, producing male and female medusae. The medusoid stage lasts between 7 -30 days (Stepanjants, 1998). Eggs and sperm are released into the sea and fertilization is external, resulting in an embryo that develops into a typical planula larva (Cornelius, 1995a, b; Gili & Hughes, 1995). In Europe, the medusae of Obelia longissima are usually found in the water somewhere between April and July, depending on area (see MarLIN review). Assuming that all the medusae survive to release gametes, Cornelius (1990b) estimated that an average colony could potentially produce about 20,000 planulae, although he also suggested that only one of these planulae was likely to survive to form a colony which itself might survive to reproduce.
  • Ulva intestinalis is a rapidly growing opportunistic species. It can be found in reproductive condition at all times of the year, but maximum development and reproduction occur during the summer months (Burrows, 1991). The life history consists of an alternation between haploid gametophytic and diploid sporophytic generations (see MarLIN review). The haploid gametophytes produce enormous numbers of biflagellate motile gametes which cluster and fuse to produce a sporophyte (diploid zygote). The sporophyte matures and produces large numbers of quadriflagellate zoospores that mature as gametophytes, and the cycle is repeated. Together spores and gametes are termed 'swarmers'. Mobility of swarmers belonging to Ulva intestinalis (studied as Enteromorpha intestinalis) can be maintained for as long as 8 days (Jones & Babb, 1968) and as a result, tend to have large dispersal shadows. Propagules have been found 35 km from the nearest adult plants (Amsler & Searles, 1980).
  • Littorina littorea can breed throughout the year but the length and timing of the breeding period are extremely dependent on climatic conditions. Fertilization is internal and Littorina littorea sheds egg capsules directly into the sea during spring tides. Eggs are released on several occasions. Fecundity can be as much as 100,000 for a large female (27 mm shell height) per year. Larval settling time or pelagic phase can be up to six weeks.
  • Spawning in Mytilus edulis is protracted in many populations, with a peak of spawning in spring and summer (see MarLIN review). Gametogenesis and spawning varies with geographic location, e.g. southern populations often spawn before more northern populations (Seed & Suchanek, 1992). The planktonic life can exceed two months in the absence of suitable substrata or optimal conditions (Bayne, 1965; Bayne, 1976a). Mytilus edulis recruitment is dependant on larval supply and settlement, together with larval and post-settlement mortality. Larval mortality is probably due to adverse environmental conditions, especially temperature, inadequate food supply, inhalation by suspension feeding adult mytilids, difficulty in finding suitable substrata and predation (Lutz & Kennish, 1992). Widdows (1991) suggested that any environmental factor that increased development time, or the time between fertilization and settlement would increase larval mortality. Jorgensen (1981) estimated that larvae suffered a daily mortality of 13% in the Isefjord, Denmark but Lutz & Kennish (1992) suggested that larval mortality was approximately 99%. Recruitment in many Mytilus sp. populations is sporadic, with unpredictable pulses of recruitment (Seed & Suchanek, 1992). Mytilus is highly gregarious and final settlement often occurs around or in-between individual mussels of established populations.
  • Semibalanus balanoides is an obligate cross-fertilising hermaphrodite. It produces one brood per year of 5000 -10,000 eggs/ brood in mature adults but this varies with age and location (see MarLIN review). Copulation takes place in the UK from November to early December and nauplii larvae are released from the barnacle between February and April, in synchronisation with the spring algal bloom. Nauplii larvae are planktotrophic and develop in the surface waters for about two months. They pass through six nauplii stages before eventually developing into a cyprid larva. Cyprid larvae are specialized for settlement and peak settlement occurs in April to May in the west and May to June in the east and north of Britain although settlement and subsequent recruitment are highly variable.

Time for community to reach maturity

LR.H is subjected to frequent small disturbances and the associated community is characterized by relatively short lived and opportunistic species. As a consequence, the time taken for the community to reach 'maturity' is likely to be fairly rapid, i.e. less than a few years.
  • Obelia longissima is capable of growing rapidly, budding and forming stolons that allow it to colonize space rapidly. Hydroids are often the first organisms to colonize available space in settlement experiments (Gili & Hughes, 1995). Rapid growth, budding and the formation of stolons allows hydroids to colonize space rapidly. Cornelius (1992) stated that Obelia longissima could form large colonies within a matter of weeks.
  • Ulva intestinalis is opportunistic and capable of rapidly colonizing bare substratum, providing the substratum is suitable. Kitching & Thain (1983), for example, reported that following the removal of the urchin Paracentrotus lividus (that grazes on the Ulva sp.) from areas of Lough Hyne, Ireland, Ulva sp. grew over the cleared area and reached a coverage of 100% within one year.
  • Littorina littorea is a slow crawler but because LR.H rockpools are likely to be surrounded by other rockpools, active immigration of snails is possible from the surrounding rocky shore where Littorina littorea may be abundant.
  • The establishment of the Mytilus edulis community may take significantly longer (see Sensitivity). However, this species is not characteristic of the biotope. Furthermore, if Mytilus edulis are present in LR.H, they will usually be part of a larger mussel bed (SLR.MytX) and this will favour recruitment to the area. Recovery of Mytilus edulis may take at least 5 years, although in certain circumstances and under some environmental conditions recovery may take significantly longer.
  • Bennell (1981) observed that barnacles were removed when the surface rock was scraped off in a barge accident at Amlwch, North Wales. Barnacle populations returned to pre-accident levels within 3 years. However, barnacle settlement and recruitment can be highly variable because they are dependent on a suite of environmental and biological factors (see MarLIN review), therefore populations may take longer to recover.

Additional information

-

Preferences & Distribution

Recorded distribution in Britain and IrelandLR.H has not been recorded in Ireland. In Scotland, it has only been recorded at Devil's Thrashing Floor, Dumfries & Galloway. On the south Devon coast it is found near Brixham. On the west coasts it has been recorded near Port Talbot in Wales and at Duddon Sands and St Bees Head in Cumbria. It has also been recorded on the north coast of Norfolk and near Blackwater Estuary in Essex.

Habitat preferences

Depth Range Mid shore
Water clarity preferences
Limiting Nutrients Data deficient
Salinity Full (30-40 psu)
Physiographic Enclosed coast / Embayment
Biological Zone Eulittoral
Substratum Cobbles, Pebbles, Gravel / shingle, Sand
Tidal
Wave Moderately exposed, Sheltered
Other preferences Enclosed coasts (inlets, harbours)

Additional Information

LR.H is found in moderately exposed to sheltered habitats. It is considered rare (Connor et al., 1997b).

Species composition

Species found especially in this biotope

    Rare or scarce species associated with this biotope

    -

    Additional information

    The MNCR reported 129 species from this biotope, although not all species occur in all examples of the biotope (JNCC, 1999).

    Sensitivity reviewHow is sensitivity assessed?

    Explanation

    The hydroid Obelia longissima is particularly characteristic to this biotope. The common periwinkle is part of the biotope name and has therefore also been listed as an important characterizing species. Ulva intestinalis, although not a characterizing species per se, is representative of other ephemeral green algae that may be found in LR.H. It also provides a food source for the common periwinkle. The common mussel Mytilus edulis has been included as another important species since it was found in almost all records of the biotope, often in abundance, and mussel patches may provide some stability to this otherwise unstable and transient biotope. The acorn barnacle Semibalanus balanoides is likely to be found attached to stones and shells. It has been listed as important 'other' since it may be common is some LR.H pools.

    Species indicative of sensitivity

    Community ImportanceSpecies nameCommon Name

    Physical Pressures

     IntoleranceRecoverabilitySensitivitySpecies RichnessEvidence/Confidence
    High Very high Low Major decline High
    The majority of the species associated with this biotope are attached permanently to the substratum and the removal of this substratum would result in the loss of the biotope. Ulva intestinalis, if detached from the substratum, may be buoyed up by gas and float to the surface where it continues to grow. However, the survival of this species in isolation will not constitute the biotope and therefore intolerance has been assessed as high. Recoverability is likely to be very high (see additional information).
    High Very high Low Major decline Moderate
    Obelia longissima forms long flexible colonies so that smothering material is likely to bend the colony flat against the substratum. In addition, local hypoxic conditions are also likely to inhibit growth. Although hydranths are likely to regress and portions of the colony are likely to die or be reabsorbed, parts of the colony are likely to become dormant, or otherwise survive for a period of at least a month. Ulva intestinalis is highly intolerant to smothering due to its filamentous form. It is likely to be completely smothered at the benchmark level and photosynthesis would be prevented due to lack of light. Furthermore, the thin fronds of the algae may start to rot. Littorina littorea will normally die if it cannot reach the surface within 24 hours (Chandrasekara & Frid, 1998). Under 5 cm of the mixed substratum associated with LR.H, it is possible that they may not reach the surface in this time. However, the journey to the surface is facilitated in well oxygenated sediments that contain fluid. The mussel Mytilus edulis and acorn barnacle Semibalanus balanoides may only be of intermediate intolerance to smothering (see MarLIN reviews) but these species are not characteristic of the biotope.

    On balance, intolerance has been assessed as high since the characterizing species are likely to experience high levels of mortality. Recoverability is expected to be very high (see additional information).

    Low Immediate Not sensitive No change Low
    An increase in suspended sediment may have a deleterious effect on the suspension feeding community in LR.H. It is likely to clog their feeding apparatus to some degree, resulting in a reduced ingestion over the benchmark period and, subsequently, a decrease in growth rate. For hydroids especially this could potentially lead to a reduction in overall biomass. Moreover, because the rockpool has a 'pulsed' influx of water, the suspended sediment is likely to settle between tides and, over the course of one month, increase the depth of sediment in the pool. Some smaller immobile species including barnacle and tubeworms may be temporarily smothered. Furthermore, hydranths toward the lower reaches of the hydroid colonies may be smothered and regress. On balance, intolerance has been assessed as low since, at most, there may be a reduction in the overall hydroid standing biomass and this will not affect the recognizable biotope. Hydroids exhibit remarkable powers of regeneration and Obelia longissima (as commissularis) rapidly heals cut ends of stolons or branches within 1-2 min, and new growth can rapidly occur from the cut end or both ends of an excised piece of stolon (Berrill, 1949). Assuming the majority of the colonies remained, recovery has been assessed as immediate.
    Tolerant* Very high Not sensitive No change Low
    A decrease in suspended sediment is likely to benefit the community associated with LR.H. The suspension feeders may be able to feed more efficiently due to a reduction in time and energy spent cleaning feeding apparatus. Over the course of the benchmark the hydroids may increase in abundance and the mussels may experience an enhanced scope for growth. Therefore, tolerant* has been suggested.
    High Very high Low Major decline Moderate
    LR.H is found in the eulittoral. Moving the biotope up one vertical biological zone on the shore, in combination with the shallow nature of the pool, could mean that this biotope has the potential to dry out, especially if this shift coincided with hot, dry or windy weather. Alternatively, the biotope would be more at risk from freezing if the shift coincided with cold temperatures and icy winds.

    Ulva intestinalis can survive several weeks of living in completely dried out rock pools, while becoming completely bleached on the uppermost layers, but remaining moist underneath the bleached fronds. The Littorina littorea may be found at the high tide level on the shore and will probably be able to find some refuge underneath the damp fronds of the Ulva intestinalis. During long periods of exposure to desiccating influences, Littorina littorea forms a dried mucus seal around the shell aperture thereby reducing evaporation. In contrast, Obelia longissima is highly intolerant desiccation and, at the benchmark level, the hydroids in LR.H are likely to experience mass mortality. Due to the fact that hydroids characterize this biotope, intolerance has been assessed as high. Even where the colonies are totally destroyed and/or removed, remaining resting stages or colony fragments, together with rapid growth and potentially good recruitment should result in rapid recovery. Recoverability has been assessed as very high.
    Intermediate Very high Low Decline Low
    An increase in emergence would mean that this shallow rockpool would be at greater risk of desiccation (see above) and extremes of temperature (see below), since the pool would be exposed to the influences of air temperature for longer. The Ulva intestinalis may dry out and become bleached in the upper reaches of the rock pool although the majority of the plants would survive. The common periwinkles could move down into the wetter reaches of the pool when the pool wasn't immersed by the tide. The hydroids would most likely experience a decline in abundance since those in the upper reaches of the pool would die if the rockpool started to dry out. Overall, the biotope would probably remain but over a smaller area. Accordingly, intolerance has been assessed as intermediate but with a very high recovery (see additional information).
    Tolerant* Not sensitive Rise Very low
    A decrease in emergence would mean that this shallow rock pool would be at less risk of desiccation. In addition, depending on the nature of the surrounding bedrock, the rockpool may become slightly deeper. As a result, it is possible that species diversity could increase as, for example, other hydroids colonized the pool. This could result in increased competition between the suspension feeders but, on the whole, LR.H is likely to be tolerant* of a decrease in emergence at the benchmark level.
    High Very high Low Major decline Very low
    LR.H is found in shallow eulittoral rock pools and is not expected to experience any water flow, unless they covered by the tide, apart from wind driven water movement. An increase in water flow rate and the benchmark level is likely to flush much of the sediment from the pool. This would result in the vast majority of the hydroids, ephemeral green algae, lugworms and sand masons being lost. The Littorina littorea, Mytilus edulis and Semibalanus balanoides may well remain but this would not constitute a recognizable biotope in terms of LR.H. Intolerance has therefore been assessed as high. Recoverability is expected to be very high.
    High Very high Low Decline Low
    LR.H is found in shallow eulittoral rock pools and is not expected to experience any water flow, unless they covered by the tide, apart from wind driven water movement. Obelia longissima and Littorina littorea have both been recorded in very weak tidal streams (no information on Ulva intestinalis) and tolerant has been suggested.
    High Very high Low Decline Moderate
    Due to the fact that LR.H is found in shallow eulittoral rockpools, the associated community must be adapted, to a certain degree, to frequent and often rapid changes in temperature. Air temperatures can be greatly elevated on hot days and due to the shallow nature of the pool, the water is likely to heat up quickly. Ulva intestinalis, Littorina littorea and Mytilus edulis all occur to the south of the British Isles and, because they are often found in upper shore rockpools, are likely to be tolerant to both chronic and acute increases in temperature. Semibalanus balanoides is pre-eminently a boreal species, adapted to cool environments. Reproduction in Semibalanus balanoides is inhibited by temperatures greater than 10 °C (Barnes, 1989) and it has been assessed as being of intermediate intolerance to an increase in temperature at the benchmark level (See MarLIN review).

    Cornelius (1995b) suggested that numerous records in the Indo-Pacific were probably attributable to Obelia longissima and it is unlikely to be adversely affected by chronic temperature change at the benchmark level within the British Isles. However, Berrill (1949) reported that hydranths did not start to develop unless the temperature was less than 20 °C. Furthermore, Berrill (1948) reported that Obelia species were absent from a buoy in July and August during excessively high summer temperatures in Booth Bay Harbour, Maine, USA and the abundance of Obelia species and other hydroids fluctuated greatly, disappearing and reappearing as temperatures rose and fell markedly above and below 20 °C during this period (see MarLIN review). Therefore it is likely that Obelia longissima is highly intolerant to an acute rise in temperature at the benchmark level since temperatures in excess of 20 °C can reasonably be expected over summer in a shallow eulittoral rockpool. As Berrill (1948) suggested, other hydroids may be equally intolerant.

    Overall, therefore, intolerance of LR.H to an acute increase in temperature has been assessed as high. Recoverability is expected to be very high (see additional information).
    Intermediate Very high Low Decline Moderate
    Due to the fact that LR.H is found in shallow eulittoral rockpools, the associated community must be adapted, to a certain degree, to frequent and often rapid changes in temperature. These pools may even freeze over during the coldest winter months.

    Kosevich & Marfenin (1986) reported that Obelia longissima was active all year round in the White Sea. Similarly, its northern limit lies in the Arctic Circle (Cornelius, 1995b; Stepanjants, 1998) suggesting that it probably tolerant of the lowest temperatures it is likely to encounter in Britain and Ireland. However, growth rates are reduced at low temperatures. Berrill (1949) reported that stolons grew, under optimal nutritive conditions, at less than 1 mm in 24 hrs at 10-12 °C, 10 mm in 24 hrs at 16-17 °C, and as much as 15-20 mm in 24 hrs at 20 °C.
    Ulva intestinalis occurs to the north of the British Isles, so is likely to be tolerant of chronic decreases in temperature at the benchmark level. Ulva sp. (as Enteromorpha) were reported to be tolerant of a temperature of -20 °C (Kylin, 1917).

    Adult Littorina littorea can easily tolerate sub-zero temperatures and the freezing of over 50% of their extracellular body fluids, although long term chronic temperature reductions may retard growth (see MarLIN review).
    Mytilus edulis can also withstand extreme cold and freezing, surviving when its tissue temperature drops to -10 °C (Williams, 1970; Seed & Suchanek, 1992) or exposed to -30°C for as long as six hours twice a day (Loomis, 1995). Bourget (1983) reported that cyclic exposure to otherwise sublethal temperatures, e.g. -8 °C every 12.4 hrs resulted in significant damage and death after 3-4 cycles. This suggests that Mytilus edulis can survive occasional, sharp frost events, but may succumb to consistent very low temperatures over a few days. Although Mytilus edulis may be intolerant of prolonged freezing temperatures, it is generally considered to be eurythermal.
    Semibalanus balanoides is pre-eminently a boreal species, adapted to cool environments. An exceptional tolerance to cold is acquired in December and January and is lost between February and April. The median lethal temperature in January was -17.6 °C in air for 18 hours, whereas animals in June could only withstand -6.0 °C (Crisp & Ritz, 1967). Semibalanus balanoides was not affected during the severe winter of 1962-63 in most areas, except the south east coast which suffered 20-100% mortality. (Crisp, 1964).

    On balance, intolerance of LR.H to a decrease in temperature at the benchmark level has been assessed as intermediate to reflect the possibility that some pool higher up the shore may freeze over. Recovery is expected to be very high (see additional information).

    Low Immediate Not sensitive No change Moderate
    An increase in turbidity may reduce primary production in the rockpool. For pools further up the shore that have less contact with the sea to replenish the water and hence suspended matter, this may lead to a reduction on ingestion for suspension feeders. Over the course of the benchmark this may lead to a reduced scope for growth and Ulva intestinalis may also experience a slight reduction in growth. Intolerance has been assessed as low with an immediate recovery.
    Tolerant* Not sensitive No change Low
    A decrease in turbidity is likely to enhance primary productivity within the biotope. This will directly benefit Ulva intestinalis and indirectly benefit Littorina littorea, Obelia longissima, Mytilus edulis and Semibalanus balanoides through secondary productivity. Bourget et al. (in press), for example, noted that for any given water temperature on buoys in the Gulf of St Lawrence, water transparency and primary production influenced the biomass of fouling organisms, including Obelia longissima. Biomass was reported to increase with increasing transparency up to a transparency of 15 m after which it decreased again (see Figure 2, Bourget et al., in press). Increased transparency was presumably correlated with increased primary production and hence food availability. Tolerant* has been recorded.
    High Very high Low Major decline Low
    An increase in wave exposure at the benchmark level is likely to adversely affect LR.H biotopes in the lower eulittoral. Both Ulva intestinalis and Littorina littorea are out of their preferred habitat in very wave exposed locations. If Littorina littorea were dislodged they are likely to be damaged, and may therefore become more susceptible to predation. Small patches of Mytilus edulis may also be susceptible to dislodgement in very exposed conditions. Dare (1976) noted that individual mussels swept or displaced from a mussel beds rarely survived, since they either became buried in sand or mud, or were scattered and eaten by oystercatchers. Obelia longissima is found in habitats with all levels of wave exposure because the branches and stems are flexible and probably able to withstand oscillatory flow (see Hunter, 1989). Semibalanus balanoides is tolerant of all levels of wave exposure. However, in LR.H pools in the lower eulittoral, very wave exposed shores would probably mean that the sediment would be flushed from the shallow pools, effectively removing the substratum (see above). In this case, the relative tolerance of Obelia longissima to increased wave exposure is irrelevant. It is likely that the entire biotope could be lost in the lower eulittoral and accordingly intolerance has been assessed as high. Recovery is expected to be very high.
    High Very high Low Decline Low
    A decrease in wave exposure is likely to adversely affect LR.H rockpools and it likely that, at the benchmark level, a different biotope will develop. The existence of LR.H is, in some respects, dependent on the influence of wave exposure. LR.H is dominated by ephemeral hydroids and seaweeds which thrive due to the disturbed nature of the habitat which prevents their competitive exclusion by late successional species. A reduction in wave exposure would remove this disturbance and therefore allow succession to take place in which the hydroids and ephemeral seaweeds would probably be out-competed by longer lived species. LR.H would be lost and, accordingly, intolerance has been assessed as high. Recoverability is expected to be very high (see additional information).
    Tolerant Not relevant Not sensitive Not relevant Moderate
    None of the important characterizing species in LR.H are thought to have effective mechanisms for detecting noise and are likely to be tolerant of noise at the benchmark level.
    Tolerant Not relevant Not sensitive Not relevant Moderate
    None of the important characterizing species in LR.H are thought to have effective mechanisms for detecting visual presence and are likely to be tolerant of visual presence at the benchmark level.
    Intermediate Very high Low Decline Low
    The existence of LR.H is, in some respects, dependent on the influence of physical disturbance such as sand scour. LR.H is dominated by ephemeral hydroids and seaweeds which thrive due to the disturbed nature of the habitat which prevents their competitive exclusion by late successional species. However, abrasion by an anchor or fishing gear could potentially destroy parts of the biotope, depending on the size of the pool and on the size off the impact. The delicate filamentous fronds of Ulva intestinalis will easily be scraped off the surface of the rock. Parts of the delicate Obelia longissima colonies are also likely to be removed. However, the surface covering of hydrorhizae may remain largely intact, from which new uprights are likely to grow. In addition, the resultant fragments of colonies may be able to develop into new colonies (see displacement). If the shells of Littorina littorea or Mytilus edulis are damaged, the risk of predation and desiccation will increase. In most cases, it is very likely that some part of each population will remain and therefore, intolerance has been assessed as intermediate. Recovery is likely to be very high (see additional information).
    Intermediate Very high Low Minor decline Moderate
    If Littorina littorea was picked up and moved somewhere else it is unlikely that it would experience any adverse effects. Despite the other two characterizing species, Obelia longissima and Ulva intestinalis, being permanently attached to the substratum, they can be remarkably tolerant of displacement if replaced in water. Fragmentation is thought to be a possible mode of asexual reproduction in hydroids (Gili & Hughes, 1995). Therefore, it is possible that a proportion of displaced colonies (or fragments thereof) may attach to new substrata and survive. Cornelius (1995b) noted that detached specimens of Obelia longissima sometimes continue to grow if entangled in the intertidal. Ulva intestinalis, if detached from the substratum, may be buoyed up by gas and float to the surface where it continues to grow. Mytilus edulis may survive displacement (see MarLIN review) but Dare (1976) noted that individual mussels swept or displaced from mussel beds rarely survived, since they either became buried in sand or mud, or were scattered and eaten by oystercatchers. Furthermore, Semibalanus balanoides will not survive displacement. However, these two species are not characteristic of the biotope and their loss would not affect the visible biotope. On balance, an intolerance of intermediate has been recorded since it is likely that some hydroid colonies may die and not all of the displaced Ulva intestinalis will survive. Recoverability will be very high (see additional information).

    Chemical Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    Intermediate High Low Decline Moderate
    • No information concerning the intolerance of Obelia longissima was found. However, evidence suggests that several species of hydroid exhibit sublethal effects due to synthetic chemical contamination and lethal effects due to TBT contamination (see MarLIN review).
    • Ulva intestinalis has been assessed to have an intermediate intolerance to synthetic chemical pollution as available evidence highlights adverse effects upon the species viability and damage leading to death (see MarLIN review). Scarlett et al. (1997) analyzed water samples taken from the Plymouth Sound locality for the presence of the s-triazine herbicide, Irgarol 1051, which is an ingredient of antifouling paints used on pleasure boats and ships. The highest detected concentration of over 120 ng/L significantly inhibited the growth of Ulva intestinalis. Following the Torrey Canyon tanker oil spill, copious amounts of solvent based detergents were sprayed directly on to the shore. Algae on the higher shore were especially affected, and included Ulva intestinalis (as Enteromorpha intestinalis in high level rock pools where it was killed (Smith, 1968).
    • Littorina littorea is tolerant of high TBT levels (Oehlmann et al., 1998) and has often been present in areas where the very TBT sensitive dog whelk Nucella lapillus has disappeared. Although imposex is rare in Littorina littorea, strong TBT contamination may affect a population significantly by reducing reproductive ability (Deutsch & Fioroni, 1996) through the development of intersex. Intersex is defined as a change in the female pallial oviduct towards a male morphological structure (Bauer et al., 1995). However, only sexually immature and juvenile individuals of Littorina littorea are able to develop intersex. Also, owing to the reproductive strategy of Littorina littorea, which reproduces by means of pelagic larvae, populations do not necessarily become extinct as a result of intersex (Casey et al., 1998).
    • The effects of contaminants on Mytilus sp. were extensively reviewed by Widdows & Donkin (1992) and Livingstone & Pipe (1992) and Mytilus edulis has been assessed as being of intermediate intolerance to synthetic chemicals (see MarLIN review)
    • Barnacles have a low resilience to chemicals such as dispersants, dependant on the concentration and type of chemical involved (Holt et al., 1995) and most Semibalanus balanoides were killed in areas treated with dispersants (Smith, 1968). However, the barnacle population suffered indirectly as a result of the mass mortality of grazers. The resultant bloom of algae, and growth of fucoids, within 6 months, grew over and killed surviving barnacles (Hawkins & Southward, 1992).
    On balance, it has been suggested that the intolerance of LR.H to synthetic chemicals is intermediate. Despite the characterizing species showing primarily sublethal effects, the nature of the rockpool, especially those higher up on the shore, may mean that the contaminant takes some time to be flushed from the biotope. This would mean the sublethal effects may manifest themselves into a more adverse reaction. Due to the uncertainty with regards to contaminants leaving the system, a recoverability of high has been suggested.
    Heavy metal contamination
    Intermediate High Low Decline Moderate
    • Although no information on the effects of heavy metals on Obelia longissima was found, evidence suggests that hydroids may suffer at least sub-lethal effects and possibly morphological changes and reduced growth due to heavy metal contamination (see MarLIN review).
    • Evidence suggests that Ulva sp. are relatively tolerant of heavy metal exposure at environmentally realistic concentrations, but experience reduced growth.
    • Most of the information available suggests that adult gastropod molluscs are rather tolerant of heavy-metal toxicity (Bryan, 1984). Winkles may absorb metals from the surrounding water by absorption across the gills or from the diet, and evidence from experimental studies on Littorina littorea suggest that the diet is the most important source (Bryan et al., 1983). Bryan et al. (1983) suggest that Littorina littorea is a reasonable bioindicator for Ag, Cd, Pb and perhaps As. It is not found to be a reliable indicator for other metals because of some interactions between metals and regulation of some, such as Cu and Zn (Langston & Zhou Mingjiang, 1986). The lethal dose of mercury (as mercury chloride) is between 1 and 10 ppm of seawater (Staines, 1996). This stems mainly from its ability to accumulate trace elements and compounds and consequential behavioural changes.
    • The effects of contaminants on Mytilus sp. were extensively reviewed by Widdows & Donkin (1992) and Livingstone & Pipe (1992). Overall, Mytilus edulis was assessed as being of intermediate intolerance to heavy metal contamination (see MarLIN review). Mussels were reported to be missing from a wider area than other shore organisms on a Cumbrian shore in the vicinity of a phosphate rich effluent outfall contaminated by a number of heavy metals (Holt et al., 1998).
    • Semibalanus balanoides is considered to be of low intolerance to heavy metal exposure (see MarLIN review).
    On balance, it has been suggested that the intolerance of LR.H to heavy metals is intermediate. Despite the characterizing species showing primarily sublethal effects, the nature of the rockpool, especially those higher up on the shore, may mean that the contaminant takes some time to be flushed from the biotope. This would mean the sublethal effects may manifest themselves into a more adverse reaction. Due to the uncertainty with regards to contaminants leaving the system, a recoverability of high has been suggested.
    Hydrocarbon contamination
    High High Moderate Major decline Moderate
    • Little information of the effects of hydrocarbons on hydroids was found although hydroid species adapted to a wide variation in environmental factors and with cosmopolitan distributions tend to be more tolerant of polluted waters (Boero, 1984; Gili & Hughes, 1995). The water soluble fractions of Monterey crude oil and drilling muds were reported to cause polyp shedding and other sublethal effects in the athecate Tubularia crocea in laboratory tests (Michel & Case, 1984; Michel et al., 1986; Holt et al., 1995). However, no information concerning the effects of hydrocarbons or oil spills on Obelia species was found.
    • Ulva intestinalis is likely to demonstrate intolerance to hydrocarbon contamination. Likely effects include smothering, inhibition of respiration and photosynthesis, bleaching, and interference with reproduction so that affected populations may be destroyed. However, the species tends to recover very rapidly from oil pollution incidents. For instance, after the Torrey Canyon tanker oil spill in 1967, grazing species were killed, and a dense flush of ephemeral green algae (such as Ulva and Blidingia sp.) appeared on the rocky shore within a few weeks and persisted for up to one year (Smith, 1968).
    • Observations from oil spills such as the Sea Empress and Amoco Cadiz suggest that gastropod molluscs are highly intolerant of hydrocarbon pollution because they become encrusted with oil and washed from the substratum where they are most likely eaten or die from desiccation (Suchanek, 1993). Given that Littorina littorea represents the most significant grazer in LR.H, it is likely that its disappearance will lead to a proliferation of ephemeral to the green algae, to the detriment of the hydroids with which the algae may compete for space.
    • A wealth of information concerning the effects of hydrocarbon contamination on Mytilus edulis was available (see MarLIN review). Overall, hydrocarbon tissue burden results in decreased scope for growth and, in some circumstances, may result in mortalities, reduced abundance or extent of the Mytilus edulis.
    • Littoral barnacles have a high resistance to oil (Holt et al., 1995). However, after the Torrey Canyon oil spill, some mortality of barnacles was caused by the oil although most had been able to form a hole in the covering of oil and were 'in good order' (Smith, 1968). Significant reductions in densities of Semibalanus balanoides were observed after the Exxon Valdez oil spill (1989) , especially at high and mid shore (Highsmith et al., 1996), although up to 98% reduction in barnacle cover resulted from treatment by hot-water washing. Experimentally, Semibalanus balanoides has been found to tolerate exposure to the water-accommodated fraction of diesel oil at 129.4 µg/l for two years (Bokn et al., 1993).
    On balance, it has been suggested that the intolerance of LR.H to hydrocarbons is high. Despite the some of characterizing species showing primarily sublethal effects, the key grazers are likely to be lost and the biotope will become smothered with fast growing algae. The nature of the rockpool, especially those higher up on the shore, may mean that the contaminant takes some time to be flushed from the biotope. This would mean the sublethal effects may manifest themselves into a more adverse reaction. Due to the uncertainty with regards to contaminants leaving the system, a recoverability of high has been suggested.
    Radionuclide contamination
    No information No information No information Insufficient
    information
    Not relevant
    Apart from Ulva intestinalis, no information was found concerning the effects of radionuclides on the characterizing and other important species in LR.H and no assessment of sensitivity has been made. Ulva sp. are known to be able to acquire large concentrations of radioactive substances from surrounding water. In the vicinity of the Sellafield nuclear plant, England, Ulva (as Enteromorpha) sp. accumulated zirconium, niobium, cerium and plutonium-239, however the species appeared to be unaffected by the radionuclides (Clark, 1997).
    Changes in nutrient levels
    Intermediate Very high Low Decline Low
    In a shallow rockpool such as those associated with LR.H, an influx of nutrients could lead to an increase in the abundance of Ulva intestinalis since nitrogen enrichment has been shown to enhance its growth (Kamer & Fong, 2001). An increase in the standing biomass of Ulva intestinalis would benefit Littorina littorea which grazes on it. Mytilus edulis may also benefit from moderate nutrient enrichment, especially in the form of organic particulates and dissolved organic material. The resultant increased food availability may increase growth rates, reproductive potential and decrease vulnerability to predators. In contrast, Obelia longissima may be competitively displaced by the Ulva intestinalis, leading to a reduction in the abundance of hydroids. In respect of the possibility of a reduction in hydroid coverage, an intermediate intolerance has been suggested. Recoverability is likely to be very high since excess nutrients are likely to be utilized quickly.
    Low Very high Very Low No change Low
    High air temperatures cause surface evaporation of water from pools, so that salinity steadily increases, especially in pools not flooded by the tide for several days. The extent of temperature and salinity change is affected by the frequency and time of day at which tidal inundation occurs. If high tide occurs in early morning and evening the diurnal temperature follows that of the air, whilst high water at midday suddenly returns the temperature to that of the sea (Pyefinch, 1943). Heavy rainfall, followed by tidal inundation can cause dramatic fluctuations in salinity, and values ranging from 5-30 psu have been recorded in rockpools over a period of 24 hrs (Ranade, 1957). As a consequence of such a regime, the entire LR.H community will be adapted, to a certain degree, to fluctuating salinities. For instance, during the summer, owing to excessive evaporation brine precipitation may occur in rockpools containing Ulva intestinalis and salinity has been reported to rise as high as 180 psu (Reed & Russell, 1979). At the benchmark level, an intolerance of low has been suggested to reflect the different experiences rockpools at the top and bottom of the eulittoral are likely to have.
    Low Very high Moderate No change Low
    High rainfall will reduce salinity in rock pools and may create a surface layer of brackish/nearly fresh water for a period. The extent of temperature and salinity change is affected by the frequency and time of day at which tidal inundation occurs. If high tide occurs in early morning and evening the diurnal temperature follows that of the air, whilst high water at midday suddenly returns the temperature to that of the sea (Pyefinch, 1943). Heavy rainfall, followed by tidal inundation can cause dramatic fluctuations in salinity, and values ranging from 5-30 psu have been recorded in rockpools over a period of 24 hrs (Ranade, 1957). As a consequence of such a regime, the entire LR.H community will be adapted, to a certain degree, to fluctuating salinities. Ulva intestinalis, for instance, is considered to be a remarkably euryhaline species, tolerant of extreme salinities ranging from 0 psu to 136 psu although reduced salinity can affect the growth rate of Ulva intestinalis. Obelia longissima, Littorina littorea and Semibalanus balanoides are also found in areas of reduced salinity. Mytilus edulis exhibits a defined behaviour to reducing salinity, initially only closing its siphons to maintain the salinity of the water in its mantle cavity, which allows some gaseous exchange and therefore maintains aerobic metabolism for longer. In extreme low salinities, e.g. resulting from storm runoff, large numbers of mussels may be killed (Keith Hiscock, pers comm.). In the long term (weeks) Mytilus edulis can acclimate to lower salinities (Almada-Villela, 1984; Seed & Suchanek, 1992; Holt et al., 1998). Almada-Villela (1984) reported that the growth rate of individuals exposed to only 13 psu reduced to almost zero but had recovered to over 80 percent of control animals within one month. Mytilus edulis can also survive considerably reduced salinities, growing as dwarf individuals at 4-5psu in the Baltic. At the benchmark level, an intolerance of low has been suggested to reflect the different experiences rockpools at the top and bottom of the eulittoral are likely to have.
    Low Immediate Not sensitive No change Low
    Hydroids mainly inhabit environments in which the oxygen concentration exceeds 5 ml/l (Gili & Hughes, 1995). Although no information was found on oxygen consumption in Obelia longissima, Sagasti et al. (2000) reported that epifaunal species (including several hydroids and Obelia bicuspidata) in the York River, Chesapeake Bay, tolerated summer hypoxic episodes of between 0.5 and 2 mg O2/l (0.36 and 1.4 ml/l) for 5-7 days at a time, with few changes in abundance or species composition.

    Littorina littorea can endure long periods of oxygen deprivation. The snails can tolerate anoxia by drastically reducing their metabolic rate down to 20% of normal (MacDonald & Storey, 1999).

    Mytilus edulis is regarded as euryoxic, tolerant of a wide range of oxygen concentrations including zero (Zwaan de & Mathieu, 1992). Diaz & Rosenberg (1995) suggest it is resistant to severe hypoxia. Adult mytilids exhibited high tolerance of anoxia and Mytilus edulis is capable of anaerobic metabolism. Jorgensen (1980) observed, by diving, the effects of hypoxia (0.2 -1 mg/l) on benthic macrofauna in marine areas in Sweden over a 3-4 week period. Mussels were observed to close their shell valves in response to hypoxia and survived for 1-2 weeks before dying (Cole et al., 1999; Jorgensen, 1980).

    Semibalanus balanoides can respire anaerobically, so it can tolerate some reduction in oxygen concentration (Newell, 1979). When placed in wet nitrogen, where oxygen stress is maximal and desiccation stress is low, Semibalanus balanoides has a mean survival time of 5 days (Barnes et al., 1963).

    No information was found concerning the effects of reduced oxygen concentration on Ulva intestinalis. On balance, Mytilus edulis and Littorina littorea are tolerant of hypoxia at the benchmark level (2 mg/l O2 for 1 week) although such a reduction in oxygen concentration will incur a metabolic cost and, hence, reduced growth. Accordingly, an intolerance of low has been recorded. Once oxygen levels return to prior levels, both species are likely to recover condition within a few weeks.

    Biological Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    No information No information No information Insufficient
    information
    Not relevant
    No information was found concerning the effects of microbial pathogens on two of the characterizing species (Ulva intestinalis and Littorina littorea) but Obelia species are infected by a number of parasites at various stages in their life cycles (see MarLIN review of Obelia longissima). However, no negative effects have been noted from such an infestation. Mytilus spp. and Semibalanus balanoides also host various microbial pathogens. Mytilus edulis host a wide variety of disease organisms, parasites and commensals from many animal and plant groups including bacteria, blue green algae, green algae, protozoa, boring sponges, boring polychaetes, boring lichen, the intermediary life stages of several trematodes, copepods and decapods (See MarLIN review of Mytilus edulis). However, Mytilus edulis and Semibalanus balanoides are not characterizing species and their viability will not affect the recognizable biotope. Overall, insufficient information was available to make an assessment of sensitivity.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    There are no alien species recorded in LR.H and no assessment of intolerance has been made.
    Intermediate Very high Low No change Low
    Of the important characterizing species, only the common periwinkle Littorina littorea is known to be targeted for extraction. This species is harvested by hand, without regulation, for human consumption. In some areas, notably Ireland, collectors have noted a reduction in the number of large snails available. Due to the shallow nature of the pools associated with LR.H and the fact they are likely to occur in accessible places, it would be easy for this species to be extracted from the biotope. However, only large individuals would be removed and smaller ones would probably be left behind. Intolerance has been assessed as intermediate with a very high recoverability as adult snails would most probably crawl from nearby rock pools (see additional information).

    The 'other' important species, Mytilus edulis, has been fished for hundreds of years although the extraction of this species is unlikely to affect the recognizable biotope. Mussel beds may be exploited by hand collection or dredging. Holt et al., (1998) suggest that when collected by hand at moderate levels using traditional skills the beds will probably retain most of their biodiversity. However, they also cite incidences of over-exploitation of easily accessible small beds by anglers for bait. Holt et al., (1998) suggest that in particular embayments over-exploitation may reduce subsequent recruitment leading to long term reduction in the population or stock.

    Not relevant Not relevant Not relevant Not relevant Not relevant

    Additional information

    Hydroids have the ability to produce dormant resting stages that are far more resistant to environmental change than the colony itself. Therefore, although colonies may be removed or destroyed, the resting stages may survive attached to the substratum. The resting stages provide a mechanism for rapid recovery.
    The medusoid and planula larval stages of Obelia longissima potentially result in significant powers of dispersal. In addition, few species of hydroids have specific substrata requirements, many are generalists, and Obelia longissima has been reported from a variety of hard substrata, together with sandy habitats (Cornelius, 1992; Cornelius, 1995b). Hydroids are also capable of asexual reproduction and many species produce dormant, resting stages that are very resistant of environmental perturbation (Gili & Hughes, 1995).
    Rapid growth, budding and the formation of stolons allows hydroids to colonize space rapidly. Cornelius (1992) stated that Obelia longissima could form large colonies within a matter of weeks. Hydroids are often the first organisms to colonize available space in settlement experiments (Gili & Hughes, 1995). For example, hydroids were reported to colonize an experimental artificial reef within less than 6 months becoming abundant in the following year (Jensen et al., 1994). In similar studies, Obelia species recruited to the bases of reef slabs within 3 months and the slab surfaces within 6 months of the slabs being placed in the marine environment in summer (Hatcher, 1998). In the St Lawrence Estuary, Canada, settlement plates immersed in June were colonized by Obelia longissima within a few months, and Obelia longissima was a dominant member of the epifauna until the following July (Brault & Bourget, 1985).
    Overall, Obelia longissima is likely to recover from damage very quickly. Even where the colonies are destroyed and/or removed, remaining resting stages or colony fragments, together with rapid growth and potentially good recruitment should result in rapid recovery.

    Ulva intestinalis is generally considered to be an opportunistic species, with an 'r-type' strategy for survival. The r-strategists have a high growth rate and high reproductive rate. The species is also capable of dispersal over a considerable distance. Ulva intestinalis is amongst the first multicellular algae to appear on substrata that have been cleared following a disturbance. Following the Torrey Canyon oil spill in March 1967, for instance, species of the genus Ulva (then Enteromorpha) rapidly recruited to areas where oil had killed the herbivores that usually grazed on them, so that a rapid greening of the rocks (owing to a thick coating of Ulva) was apparent by mid-May (Smith, 1968). The rapid recruitment of Ulva to areas cleared of herbivorous grazers was also demonstrated by Kitching & Thain (1983). Following the removal of the urchin Paracentrotus lividus from areas of Lough Hyne, Ireland, Ulva (as Enteromorpha) grew over the cleared area and reached a coverage of 100% within one year. Therefore, evidence suggests that Ulva intestinalis is likely to have a considerable ability for recovery within a year.

    In the common periwinkle, the larvae form the main mode of dispersal. Littorina littorea is an iteroparous breeder with high fecundity that lives for several years. Breeding can occur throughout the year and the planktonic larval stage is long (up to 6 weeks) although larvae do tend to remain in waters close to the shore. Therefore recruitment and subsequent recovery rates should be high. Although adult immigration is usually an unlikely means of recovery, given their slow crawling, it may be possible in LR.H due to the likelihood of similar rockpools and Littorina littorea populations in close proximity.

    Seed & Suchanek (1992) reviewed studies of recovery of 'gaps' (naturally or artificially induced) in mussel beds in Mytilus species. On rocky shores, gaps are often colonized by barnacles and fucoids, barnacles enhancing subsequent recruitment of mussels. Cycles of loss and recruitment leads to a patchy distribution of mussels on rocky shores. High intertidal and less exposed sites recovered slower than low shore, more exposed sites. Overall, Mytilus spp. populations were considered to have a strong ability to recover from environmental disturbance (Seed & Suchanek, 1992; Holt et al., 1998). Larval supply and settlement could potentially occur annually but settlement is sporadic with unpredictable pulses of recruitment (Lutz & Kennish, 1992; Seed & Suchanek, 1992). Therefore, while good annual recruitment is possible, recovery may take at least 5 years, although in certain circumstances and under some environmental conditions recovery may take significantly longer.
    Bennell (1981) recorded recovery of Semibalanus balanoides populations within 3 years on a site cleared of barnacles in North Wales. Barnacle recruitment is, however, dependent on a suite of environmental and biological factors and, therefore, populations may take longer to recover.

    However, neither Mytilus edulis nor Semibalanus balanoidesare important characteristic species. For the three important characterizing species (Obelia longissima, Ulva intestinalis and Littorina littorea), recovery is likely to be very high.

    Importance review

    Policy/Legislation

    Habitats Directive Annex 1Reefs

    Exploitation

    Both Littorina littorea and Mytilus edulis are targeted for extraction. Littorina littorea is gathered by hand at a number of localities, particularly in Scotland and in Ireland where the industry is valued at around £5 million per year.

    Mussels have been harvested for food and bait since early times. British mussel production is relatively small, comprising only 5% of total Europe Community production (Edwards, 1997). Wild mussel fisheries are found in tidal flats of The Wash, Morecambe Bay, Solway and Dornoch Firths in Scotland and river estuaries such as Conwy, North Wales and the Teign and Taw, Devon (Edwards, 1997). Edwards (1997) notes that the commercial development of natural beds is hampered by sporadic and unpredictable recruitment. Extraction of Mytilus edulis from LR.H will most likely be by hand on a small scale.

    Additional information

    -

    Bibliography

    1. Albrecht, A.S., 1998. Soft bottom versus hard rock: Community ecology of macroalgae on intertidal mussel beds in the Wadden Sea. Journal of Experimental Marine Biology and Ecology229 (1), 85-109.
    2. Almada-Villela P.C., 1984. The effects of reduced salinity on the shell growth of small Mytilus edulis L. Journal of the Marine Biological Association of the United Kingdom64, 171-182.
    3. Amsler, C.D. & Searles, R.B., 1980. Vertical distribution of seaweed spores in a water column off shore of North Carolina. Journal of Phycology, 16, 617-619.
    4. Barnes, H., Finlayson, D.M. & Piatigorsky, J., 1963. The effect of desiccation and anaerobic conditions on the behaviour, survival and general metabolism of three common cirripedes. Journal of Animal Ecology, 32, 233-252.
    5. Barnes, M., 1989. Egg production in Cirripedia. Oceanography and Marine Biology: an Annual Review, 27, 91-166.
    6. Bauer, B., Fioroni, P., Ide, I., Liebe, S., Oehlmann, J., Stroben, E. & Watermann, B., 1995. TBT effects on the female genital system of Littorina littorea: a possible indicator of tributyl tin pollution. Hydrobiologia, 309, 15-27.
    7. Bayne, B.L., 1965. Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia, 2, 1-47.
    8. Bayne, B.L., 1976a. The biology of mussel larvae. In Marine mussels: their ecology and physiology (ed. B.L. Bayne), pp. 81-120. Cambridge: Cambridge University Press. [International Biological Programme 10.]
    9. Bennell, S.J., 1981. Some observations on the littoral barnacle populations of North Wales. Marine Environmental Research, 5, 227-240.
    10. Bergahn, R. & Offerman, U. 1999. Laboratory investigations on larval development, motility and settlement of white weed (Sertularia cupressina L.) - in view of its assumed decrease in the Wadden Sea. Hydrobiogia, 392(2), 233–239.
    11. Berrill, N.J., 1948. A new method of reproduction in Obelia. Biological Bulletin, 95, 94-99.
    12. Berrill, N.J., 1949. The polymorphic transformation of Obelia. Quarterly Journal of Microscopical Science, 90, 235-264.
    13. Boero, F., 1984. The ecology of marine hydroids and effects of environmental factors: a review. Marine Ecology, 5, 93-118.
    14. Bokn, T.L., Moy, F.E. & Murray, S.N., 1993. Long-term effects of the water-accommodated fraction (WAF) of diesel oil on rocky shore populations maintained in experimental mesocosms. Botanica Marina, 36, 313-319.
    15. Bourget, E., 1983. Seasonal variations of cold tolerance in intertidal molluscs and their relation to environmental conditions in the St. Lawrence Estuary. Canadian Journal of Zoology, 61, 1193-1201.
    16. Bradshaw, C., Veale, L.O., Hill, A.S. & Brand, A.R., 2002. The role of scallop-dredge disturbance in long-term changes in Irish Sea benthic communities: a re-analysis of an historical dataset. Journal of Sea Research, 47, 161-184.
    17. Brault, S. & Bourget, E., 1985. Structural changes in an estuarine subtidal epibenthic community: biotic and physical causes. Marine Ecology Progress Series, 21, 63-73.
    18. Bryan, G.W., 1984. Pollution due to heavy metals and their compounds. In Marine Ecology: A Comprehensive, Integrated Treatise on Life in the Oceans and Coastal Waters, vol. 5. Ocean Management, part 3, (ed. O. Kinne), pp.1289-1431. New York: John Wiley & Sons.
    19. Bryan, G.W., Langston, W.J., Hummerstone, L.G., Burt, G.R. & Ho, Y.B., 1983. An assessment of the gastropod Littorina littorea (L.) as an indicator of heavy metal contamination in United Kingdom estuaries. Journal of the Marine Biological Association of the United Kingdom, 63, 327-345.
    20. Burrows, E.M., 1991. Seaweeds of the British Isles. Volume 2. Chlorophyta. London: British Museum (Natural History).
    21. Casey, J.D., De Grave, S. & Burnell, G.M., 1998. Intersex and Littorina littorea in Cork Harbour: results of a medium-term monitoring programme. Hydrobiologia, 378, 193-197.
    22. Chandrasekara, W.U. & Frid, C.L.J., 1998. A laboratory assessment of the survival and vertical movement of two epibenthic gastropod species, Hydrobia ulvae, (Pennant) and Littorina littorea (Linnaeus), after burial in sediment. Journal of Experimental Marine Biology and Ecology, 221, 191-207.
    23. Clark, R.B., 1997. Marine Pollution, 4th ed. Oxford: Carendon Press.
    24. 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/
    25. 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,
    26. Connor, D.W., Brazier, D.P., Hill, T.O., & Northen, K.O., 1997b. Marine biotope classification for Britain and Ireland. Vol. 1. Littoral biotopes. Joint Nature Conservation Committee, Peterborough, JNCC Report no. 229, Version 97.06., Joint Nature Conservation Committee, Peterborough, JNCC Report No. 230, Version 97.06.
    27. Cornelius, P.F.S., 1990b. Evolution of leptolid life-cycles (Cnidaria: Hydroida). Journal of Natural History, 24, 579-594.
    28. Cornelius, P.F.S., 1992. Medusa loss in leptolid Hydrozoa (Cnidaria), hydroid rafting, and abbreviated life-cycles among their remote island faunae: an interim review.
    29. Cornelius, P.F.S., 1995a. North-west European thecate hydroids and their medusae. Part 1. Introduction, Laodiceidae to Haleciidae. Shrewsbury: Field Studies Council. [Synopses of the British Fauna no. 50]
    30. Cornelius, P.F.S., 1995b. North-west European thecate hydroids and their medusae. Part 2. Sertulariidae to Campanulariidae. Shrewsbury: Field Studies Council. [Synopses of the British Fauna no. 50]
    31. Crisp, D.J. & Ritz, D.A., 1967. Changes in temperature tolerance of Balanus balanoides during its life cycle. Helgolander Wissenschaftliche Meeresuntersuchungen, 15, 98-115.
    32. Crisp, D.J. (ed.), 1964. The effects of the severe winter of 1962-63 on marine life in Britain. Journal of Animal Ecology, 33, 165-210.
    33. Dame, R.F.D., 1996. Ecology of Marine Bivalves: an Ecosystem Approach. New York: CRC Press Inc. [Marine Science Series.]
    34. Dare, P.J., 1976. Settlement, growth and production of the mussel, Mytilus edulis L., in Morecambe Bay, England. Fishery Investigations, Ministry of Agriculture, Fisheries and Food, Series II, 28 , 25pp.
    35. Davies, C.E. & Moss, D., 1998. European Union Nature Information System (EUNIS) Habitat Classification. Report to European Topic Centre on Nature Conservation from the Institute of Terrestrial Ecology, Monks Wood, Cambridgeshire. [Final draft with further revisions to marine habitats.], Brussels: European Environment Agency.
    36. Deutsch, U. & Fioroni, P., 1996. Effects of tributyltin (TBT) and testosterone on the female genital system in the mesogastropod Littorina littorea (Prosobranchia). Helgolander Meeresuntersuchungen, 50, 105-115.
    37. Diaz, R.J. & Rosenberg, R., 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology: an Annual Review, 33, 245-303.
    38. Edwards, E., 1997. Molluscan fisheries in Britain. In The History, Present Condition, and Future of the Molluscan Fisheries of North and Central American and Europe, vol. 3, Europe, (ed. C.L. MacKenzie, Jr., V.G. Burrell, Jr., Rosenfield, A. & W.L. Hobart). National Oceanic and Atmospheric Administration, NOAA Technical Report NMFS 129.
    39. Gili, J-M. & Hughes, R.G., 1995. The ecology of marine benthic hydroids. Oceanography and Marine Biology: an Annual Review, 33, 351-426.
    40. Hatcher, A.M., 1998. Epibenthic colonization patterns on slabs of stabilised coal-waste in Poole Bay, UK. Hydrobiologia, 367, 153-162.
    41. Hawkins, S.J. & Southward, A.J., 1992. The Torrey Canyon oil spill: recovery of rocky shore communities. In Restoring the Nations Marine Environment, (ed. G.W. Thorpe), Chapter 13, pp. 583-631. Maryland, USA: Maryland Sea Grant College.
    42. Hayden, H.S., Blomster, J., Maggs, C.A., Silva, P.C., Stanhope, M.J. & Waaland, J.R., 2003. Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. European Journal of Phycology, 38, 277-294.
    43. Hayward, P.J. & Ryland, J.S. 1994. The marine fauna of the British Isles and north-west Europe. Volume 1. Introduction and Protozoans to Arthropods. Oxford: Clarendon Press.
    44. Highsmith, R.C., Rucker, T.L., Stekoll, M.S., Saupe, S.M., Lindeberg, M.R., Jenne, R.N. & Erickson, W.P., 1996. Impact of the Exxon Valdez oil spill on intertidal biota. In Proceedings of the Exxon Valdez Oil Spill Symposium. American Fisheries Society Symposium, no. 18, Anchorage, Alaska, USA, 2-5 February 1993, (ed. S.D. Rice, R.B. Spies, D.A., Wolfe & B.A. Wright), pp.212-237.
    45. 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.
    46. Holt, T.J., Rees, E.I., Hawkins, S.J. & Seed, R., 1998. Biogenic reefs (Volume IX). An overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scottish Association for Marine Science (UK Marine SACs Project), 174 pp.
    47. Huggett, J. & Griffiths, C.L., 1986. Some relationships between elevation, physico-chemical variables and biota of intertidal rockpools. Marine Ecology Progress Series, 29, 198-197.
    48. Hunter, T., 1989. Suspension feeding in oscillating flow: the effect of colony morphology and flow regime on plankton capture by the hydroid Obelia longissima. Biological Bulletin, 176, 41-49.
    49. Jensen, A.C., Collins, K.J., Lockwood, A.P.M., Mallinson, J.J. & Turnpenny, W.H., 1994. Colonization and fishery potential of a coal-ash artificial reef, Poole Bay, United Kingdom. Bulletin of Marine Science, 55, 1263-1276.
    50. Jones, W.E. & Babb, M.S., 1968. The motile period of swarmers of Enteromorpha intestinalis (L.) Link. British Phycological Bulletin, 3, 525-528.
    51. Jorgensen, B.B., 1980. Seasonal oxygen depletion in the bottom waters of a Danish fjord and its effect on the benthic community. Oikos, 32, 68-76.
    52. Jørgensen, C.B., 1981. Mortality, growth, and grazing impact on a cohort of bivalve larvae, Mytilus edulis L. Ophelia, 20, 185-192.
    53. Kamer, K. & Fong, P., 2001. Nitrogen enrichment ameliorates the negative effects of reduced salinity on green macroalga Enteromorpha intestinalis. Marine Ecology Progress Series, 218, 87-93.
    54. Kitching, J.A. & Thain, V.M., 1983. The ecological impact of the sea urchin Paracentrotus lividus (Lamarck) in Lough Ine, Ireland. Philosophical Transactions of the Royal Society of London, Series B, 300, 513-552.
    55. Kosevich, I.A. & Marfenin, N.N., 1986. Colonial morphology of the hydroid Obelia longissima (Pallas, 1766) (Campanulariidae). Vestnik Moskovskogo Universiteta Seriya Biologiya, 3, 44-52.
    56. Kylin, H., 1917. Kalteresistenze der Meerealen. Bericht der Deutschen Botanischen Gesellschafter, 35, 370-384.
    57. Langston, W.J. & Zhou Mingjiang, 1986. Evaluation of the significance of metal-binding proteins in the gastropod Littorina littorea. Marine Biology, 92, 505-515.
    58. Lersten, N.R. & Voth, P.D., 1960. Experimental control of zoid discharge and rhizoid formation in the green alga Enteromorpha. Botanical Gazette, 122, 33-45.
    59. Lewis, J.R., 1964. The Ecology of Rocky Shores. London: English Universities Press.
    60. Livingstone, D.R. & Pipe, R.K., 1992. Mussels and environmental contaminants: molecular and cellular aspects. In The mussel Mytilus: ecology, physiology, genetics and culture, (ed. E.M. Gosling), pp. 425-464. Amsterdam: Elsevier Science Publ. [Developments in Aquaculture and Fisheries Science, no. 25]
    61. Loomis, S.A., 1995. Freezing tolerance of marine invertebrates. Oceanography and Marine Biology: an Annual Review, 33, 337-350.
    62. Lutz, R.A. & Kennish, M.J., 1992. Ecology and morphology of larval and early larval postlarval mussels. In The mussel Mytilus: ecology, physiology, genetics and culture, (ed. E.M. Gosling), pp. 53-85. Amsterdam: Elsevier Science Publ. [Developments in Aquaculture and Fisheries Science, no. 25]
    63. MacDonald, J. A. & Storey, K. B., 1999. Cyclic AMP-dependent protein kinase: role in anoxia and freezing tolerance of the marine periwinkle Littorina littorea. Marine Biology, 133, 193-203.
    64. Mainwaring, K., Tillin, H. & Tyler-Walters, H., 2014. Assessing the sensitivity of blue mussel beds to pressures associated with human activities. Joint Nature Conservation Committee, JNCC Report No. 506., Peterborough, 96 pp.
    65. Michel, W.C. & Case, J.F., 1984. Effects of a water-soluble petroleum fraction on the behaviour of the hydroid coelenterate Tubularia crocea. Marine Environmental Research, 13, 161-176.
    66. Michel, W.C., Sanfilippo, K. & Case, J.F., 1986. Drilling mud evoked hydranth shedding in the hydroid Tubularia crocea. Marine Pollution Bulletin, 17, 415-419.
    67. Newell, R.C., 1979. Biology of intertidal animals. Faversham: Marine Ecological Surveys Ltd.
    68. Niesenbaum R.A., 1988. The ecology of sporulation by the macroalga Ulva lactuca L. (chlorophyceae). Aquatic Botany, 32, 155-166.
    69. Oehlmann, J., Bauer, B., Minchin, D., Schulte-Oehlmann, U., Fioroni, P. & Markert, B., 1998. Imposex in Nucella lapillus and intersex in Littorina littorea: interspecific comparison of two TBT- induced effects and their geographical uniformity. Hydrobiologia, 378, 199-213
    70. Pyefinch, K. A., 1943. The intertidal ecology of Bardsey Island, North Wales, with special reference to the recolonization of rock surfaces, and the rock pool environment. Journal of Animal Ecology, 12, 82-108.
    71. Ranade, M.R., 1957. Observations on the resistance of Tigriopus fulvus (Fischer) to changes in temperature and salinity. Journal of the Marine Biological Association of the United Kingdom, 36, 115-119.
    72. Reed, R.H. & Russell, G., 1979. Adaptation to salinity stress in populations of Enteromorpha intestinalis (L.) Link. Estuarine and Coastal Marine Science, 8, 251-258.
    73. Robles, C., 1982. Disturbance and predation in an assemblage of herbivorous Diptera and algae on rocky shores. Oecologia, 54 (1), 23-31.
    74. Sagasti, A., Schaffner, L.C. & Duffy, J.E., 2000. Epifaunal communities thrive in an estuary with hypoxic episodes. Estuaries, 23, 474-487.
    75. Scarlett, A., Donkin, M.E., Fileman, T.W. & Donkin, P., 1997. Occurrence of the marine antifouling agent Irgarol 1051 within the Plymouth Sound locality: implications for the green macroalga Enteromorpha intestinalis. Marine Pollution Bulletin, 38, 645-651.
    76. Seed, R. & Suchanek, T.H., 1992. Population and community ecology of Mytilus. In The mussel Mytilus: ecology, physiology, genetics and culture, (ed. E.M. Gosling), pp. 87-169. Amsterdam: Elsevier Science Publ. [Developments in Aquaculture and Fisheries Science, no. 25.]
    77. Smith, G.M., 1947. On the reproduction of some Pacific coast species of Ulva. American Journal of Botany, 34, 80-87.
    78. Smith, J.E. (ed.), 1968. 'Torrey Canyon'. Pollution and marine life. Cambridge: Cambridge University Press.
    79. Sommer, C., 1992. Larval biology and dispersal of Eudendrium racemosum (Hydrozoa, Eudendriidae). Scientia Marina, 56, 205-211. [Proceedings of 2nd International Workshop of the Hydrozoan Society, Spain, September 1991. Aspects of hydrozoan biology (ed. J. Bouillon, F. Cicognia, J.M. Gili & R.G. Hughes).]
    80. Staines, A., 1996. Ultrastructural study on the accumulation of mercury by Littorina littorea. http://www.csulb.edu/~zedmason/emprojects/stains/STAINS.html, 2000-05-17
    81. Stepanjants, S.D., 1998. Obelia (Cnidaria, Medusozoa, Hydrozoa): phenomenon, aspects of investigations, perspectives for utilization. Oceanography and Marine Biology: an Annual Review, 36, 179-215.
    82. Suchanek, T.H., 1993. Oil impacts on marine invertebrate populations and communities. American Zoologist, 33, 510-523.
    83. Tillin, H. & Tyler-Walters, H., 2014. Assessing the sensitivity of subtidal sedimentary habitats to pressures associated with marine activities. Phase 2 Report – Literature review and sensitivity assessments for ecological groups for circalittoral and offshore Level 5 biotopes. JNCC Report No. 512B,  260 pp.
    84. Vermaat J.E. & Sand-Jensen, K., 1987. Survival, metabolism and growth of Ulva lactuca under winter conditions: a laboratory study of bottlenecks in the life cycle. Marine Biology, 95 (1), 55-61.
    85. Widdows, J. & Donkin, P., 1992. Mussels and environmental contaminants: bioaccumulation and physiological aspects. In The mussel Mytilus: ecology, physiology, genetics and culture, (ed. E.M. Gosling), pp. 383-424. Amsterdam: Elsevier Science Publ. [Developments in Aquaculture and Fisheries Science, no. 25]
    86. Widdows, J., 1991. Physiological ecology of mussel larvae. Aquaculture, 94, 147-163.
    87. Williams, R.J., 1970. Freezing tolerance in Mytilus edulis. Comparative Biochemistry and Physiology, 35, 145-161
    88. Zwaan de, A. & Mathieu, M., 1992. Cellular biochemistry and endocrinology. In The mussel Mytilus: ecology, physiology, genetics and culture, (ed. E.M. Gosling), pp. 223-307. Amsterdam: Elsevier Science Publ. [Developments in Aquaculture and Fisheries Science, no. 25]

    Citation

    This review can be cited as:

    Marshall, C.E. 2005. Hydroids, ephemeral seaweeds and Littorina littorea in shallow eulittoral mixed substrata pools. 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/54

    Last Updated: 25/02/2005