|Researched by||Dr Heidi Tillin & Georgina Budd||Refereed by||This information is not refereed.|
Rockpools in the littoral fringe or upper eulittoral zone subject to widely fluctuating temperatures and salinity are characterized by ephemeral green alga of the genus Ulva, along with Cladophora spp. and Ulva lactuca. Due to the physical stress imposed on these upper shore pools, grazing molluscs such as the limpet Patella vulgata and the winkles Littorina littorea and Littorina saxatilis are generally in lower abundance than eulittoral pools, allowing the green seaweeds to proliferate under reduced grazing pressures. The bright orange copepod Tigriopus fulvus is tolerant of large salinity fluctuations and may occur in large numbers in these upper shore pools, along with gammarid amphipods (JNCC, 2015).
No text entered.
- none -
|Depth Range||Upper shore|
|Water clarity preferences||Data deficient|
|Limiting Nutrients||Nitrogen (nitrates), Phosphorus (phosphates)|
|Salinity||Full (30-40 psu), Variable (18-40 psu)|
|Biological Zone||Supralittoral, Upper eulittoral|
|Wave||Exposed, Moderately exposed, Sheltered, Very exposed|
No text entered.
The characteristic elements of this biotope were defined based on the description by Connor et al. (2004). This is a rock pool biotope found high on shores in the littoral fringe or upper eulittoral zone. The biotope is subject to widely fluctuating temperatures and salinity and is characterized by ephemeral green alga of the genus Ulva, including Ulva lactuca along with Cladophora spp. including Cladophora rupestris. The genus Ulva currently contains 23 taxonomically accepted species (Guiry & Guiry, 2015), although the genus is now more generally accepted as a synonym for Ulva (Hayden et al., 2003). Identification of Ulva to the species level can be problematic and in some instances species can only be distinguished by experts or by genetic analysis and understanding of the taxonomic relationships between green algal species and higher taxonomic levels is rapidly evolving.
Due to the physical stress imposed on these upper shore pools, grazing molluscs such as the limpet Patella vulgata and the winkles Littorina littorea and Littorina saxatilis are generally in lower abundance than eulittoral pools, allowing the green seaweeds to proliferate under reduced grazing pressures. The bright orange copepod Tigriopus fulvus is tolerant of large salinity fluctuations and may occur in large numbers in these upper shore pools, along with gammarid amphipods.
The sensitivity assessments are largely based on the typical characterizing species Ulva lactuca, Ulva intestinalis (formerly Enteromorpha intestinalis) and Cladophora spp. Due to the high levels of stress, the biotope is species poor and animals that do occur in the biotope are found in low abundances. The biotope is maintained by environmental stressors, common to rockpools high on the shore, including widely fluctuating temperature and salinity and these factors are considered within the sensitivity assessments where they may be altered by the pressure. As the low abundance of the grazers Patella vulgata and winkles Littorina littorea or Littorina saxatilis, allows the green algae to thrive, their sensitivity is discussed but not specifically considered within the biotope assessments. However, where the pressure may allow these species to increase in abundance then this is indicated as it may alter the character of the biotope.
The Ulva spp. and Cladophora spp. that characterize this biotope are classified as opportunistic species that are able to rapidly colonise newly created gaps across a range of sediment types, shore heights, wave exposures and salinity regimes. The life history characteristics that support this opportunism are the broad tolerances for a wide range of conditions (Vermaat & Sand-Jensen, 1987) and high growth and reproduction rates. Ulva sp. release zoospores and gametes (collectively called swarmers) to the water column in high numbers. Ulva spp. can form the swarmers from normal thallus cells that are transformed into reproductive tissue rather than having to produce specialised reproductive structures (Lersten & Voth, 1960), so that a significant portion of the macroalga's biomass is allocated to the formation of zoospores and gametes (Niesenbaum, 1988). Ulva sp. have extended reproduction periods (Smith, 1947) and swarmers are capable of dispersal over a considerable distance. For instance, Amsler & Searles (1980) showed that swarmers of a coastal population of Ulva (as Enteromorpha) reached exposed artificial substrata on a submarine plateau 35 km away. In addition to recruitment by swarmers, new growth of Cladophora rupestris may arise from the resistant multicellular branching rhizoids (van den Hoek, 1982) that may remain in situ.
The supply of swarmers in vast numbers to the coastline (Niesenbaum, 1988) is reflected in the fast recovery rates of this genus. Ulva intestinalis is amongst the first multicellular algae to appear on substrata that have been cleared following a disturbance, e.g. following the Torrey Canyon oil spill in March 1967, species of the genus Ulva 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 spp.) was apparent by mid-May (Smith, 1968). The rapid recruitment of Ulva spp. 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 grew over the cleared area and reached a coverage of 100% within one year.
Recovery of the copepod Tigriopus fulvus would be expected to be rapid (presuming a residual or localized population remained from which to recruit) as the species is in reproductive condition all year round and reaches sexual maturity within two months. It also can produce more than one brood from one fertilization. Other species that are associated with this biotope, including the limpet Patella vulgata and littorinds generally have slower recovery rates than Ulva spp. due to episodic recruitment and slower growth. Where individuals are removed from a small area, adult limpets and Littorina saxatilis may recolonize from surrounding patches of habitat where these are present. The barnacles and limpets and the winkle Littorina littorea are common, widespread species that spawn annually producing pelagic larvae that can disperse over long distances. It is therefore likely that adjacent populations will provide high numbers of larvae, although recruitment may be low due to habitat unsuitability and the presence of dense Ulva spp. preventing settlement on rock surfaces. Littorina saxatilis however brood young and do not have a pelagic life stage, recovery will therefore depend on the presence of adults in close proximity to impacted areas. As the associated species occur at low densities when they are present, their absence will not substantially alter the character of the biotope. They are therefore, not specifically considered within the resilience assessments as the biotope can be considered to have recovered before these species re-establish. Indeed, as limpets and littorinds graze on the macroalgae characterizing the biotope and can prevent blooms of Ulva spp. forming (Robles, 1982, Albrecht, 1998), their presence in large numbers would alter the character of this biotope.
Resilience assessment. The high recovery potential of the Ulva spp. and Cladophora spp. that characterize this biotope, mean that recovery is assessed as ‘High’ (within 2 years) for any level of perturbation (where resistance is ‘None’, ‘Low’, ‘Medium’ or ‘High’. Depending on the season of the impact and level of recovery, the biotope may have recovered within less than six months.
NB: The resilience and the ability to recover from human induced pressures is a combination of the environmental conditions of the site, the frequency (repeated disturbances versus a one off event) and the intensity of the disturbance. Recovery of impacted populations will always be mediated by stochastic events and processes acting over different scales including, but not limited to, local habitat conditions, further impacts and processes such as larval-supply and recruitment between populations. Full recovery is defined as the return to the state of the habitat that existed prior to impact. This does not necessarily mean that every component species has returned to its prior condition, abundance or extent but that the relevant functional components are present and the habitat is structurally and functionally recognisable as the initial habitat of interest. It should be noted that the recovery rates are only indicative of the recovery potential.
Intertidal species are exposed to extremes of high and low air temperatures during periods of emersion. They must also be able to cope with sharp temperature fluctuations over a short period of time during the tidal cycle. In winter air temperatures are colder than the sea, conversely in summer air temperatures are much warmer than the sea. Species that occur in this intertidal biotope are therefore generally adapted to tolerate a range of temperatures. In general, the water temperature of rockpools follows that of the air more closely than that of the sea, and throughout any 24 hour period, dramatic changes in temperature may be observed. For instance, Pyefinch (1943) plotted diurnal changes in a pool lying above mean high water during July. When the pool was out of contact with the sea, water temperature increased by 5°C from 14 to 19°C over a three hour period and decreased suddenly to 14°C within 1.5 hours when the incoming tide reached it. Hence, the community that inhabits such environments needs to be especially tolerant of acute temperature changes.
The key characterizing Ulva spp. are distributed globally and occur in warmer waters than those surrounding the UK suggesting that they can withstand increases in temperature at the pressure benchmark. Ulva spp. are characteristic of upper shore rock pools, where water and air temperatures are greatly elevated on hot days. Empirical evidence for thermal tolerance to anthropogenic increases in temperature is provided by the effects of heated effluents on rocky shore communities in Maine, USA. Ascophyllum and Fucus were eliminated from a rocky shore heated to 27-30°C by a power station whilst Ulva intestinalis (as Enteromorpha intestinalis) increased significantly near the outfall (Vadas et al., 1976) and Lüning (1984) reported that Cladophora rupestris could survive exposure to temperatures in the range 0 - 28°C for at least a week.
The copepod Tigriopus fulvus is more tolerant of high temperatures at higher salinities . At a salinity of 34 psu, the death point of Tigriopus fulvus is reached at 32°C (Goss-Custard et al.,1979). Limpets, Patella vulgata and littorinids may occur at low densities in this biotope. Laboratory studies suggest that adults of these species can tolerate temperature increases. The median upper lethal temperature limit in laboratory tests on Littorina littorea, Littorina saxatilis was approximately 35°C (Davenport & Davenport, 2005). Patella vulgata can also tolerate high temperatures. The body temperature of Patella vulgata can exceed 36°C in the field, (Davies, 1970); adults become non-responsive at 37-38°C and die at temperatures of 42°C (Evans, 1948). Although adults may be able to withstand acute and chronic increases in temperature at the pressure benchmark, increased temperatures may have sub-lethal effects on the population by impacting the success of reproduction phases. The distribution of Patella vulgata is 'northern' with their range extending to the Arctic circle. Populations in the southern part of England are relatively close to the southern edge of their geographic range. Increased temperatures may alter spawning cues and reproduction success in Patella vulgata populations. Observations suggest that spawning is initiated in autumn storms with greater wave action when seawater temperatures drop below 12°C (Bowman 1985; Bowman & Lewis; 1986; LeQuesne, 2005). In Northern Portugal, warming seas appear to be linked to a shortening of the reproductive period and the lack of multiple spawning events in Patella vulgata and other northern species (Ribeiro et al., 2009).
Sensitivity assessment. Adults of the associated species Patella vulgata and Littorina spp. are considered likely to be able to tolerate an acute or chronic increase in temperature at the pressure benchmark, although the timing of acute and chronic increases would alter the degree of impact and hence sensitivity. An acute change occurring on the hottest day of the year and exceeding thermal tolerances would lead to mortality. Sensitivity of Patella vulgata to longer-term, broad-scale perturbations would potentially be greater due to effects on reproduction but these changes may lead to species replacements and are not considered to significantly affect the character of the biotope. Ulva spp., are the key characterizing elements that define this biotope and are considered to tolerate increases in temperature at the pressure benchmark. Biotope resistance is, therefore, assessed as ‘High’ and recovery as ‘High’ (by default) so that the biotope is assessed as ‘Not sensitive’.
Many intertidal species are tolerant of freezing conditions as they are exposed to extremes of low air temperatures during periods of emersion. They must also be able to cope with sharp temperature fluctuations over a short period of time during the tidal cycle. In winter air temperatures are colder than the sea, conversely in summer air temperatures are much warmer than the sea. Species that occur in the intertidal are therefore generally adapted to tolerate a range of temperatures, with the width of the thermal niche positively correlated with the height of the shore that the animal usually occurs at (Davenport & Davenport, 2005).
The key species characterizing this biotope, Ulva intestinalis and Ulva lactuca are found in Arctic regions (Guiry & Guiry, 2015 and references therein), Ulva sp. (as Enteromorpha) were reported to be tolerant of a temperature of -20°C (Kylin, 1917). Vermaat & Sand-Jensen (1987) found that rapid deep freezing of Ulva lactuca collected in Roskilde Fjord, Denmark killed the plants. However, individuals from the same area when collected from frozen ice, survived and resumed growth, the plants are able to survive more gradual natural freezing (Vermaat & Sand-Jensen, 1987).
Limpets, Patella vulgata and littorinids may occur at low densities in this biotope. Laboratory studies suggest that adults of these species can tolerate temperature decreases. The median lower lethal temperature tolerances of Littorina saxatilis and Littorina littorea were -16.4 and -13 oC for individuals collected in winter from Great Cumbrae, Scotland was -14.6 oC (Davenport & Davenport, 2005). In experiments Littorina littorea were able to tolerate temperatures down to -8 °C for 8 days (Murphy, 1983). In colder conditions an active migration may occur down the shore to a zone where exposure time to the air (and hence time in freezing temperatures) is less. The limpet, Patella vulgata can also tolerate long periods of exposure to the air and can consequently withstand wide variations in temperature. Adults are also largely unaffected by short periods of extreme cold. Ekaratne & Crisp (1984) found adult limpets continuing to grow over winter when temperatures fell to -6°C, and stopped only by still more severe weather. However, loss of adhesion after exposure to -13°C has been observed with limpets falling off rocks and therefore becoming easy prey to crabs or birds (Fretter & Graham, 1994). In the very cold winter of 1962-3 when temperatures repeatedly fell below 0 °C over a period of 2 months large numbers of Patella vulgata were found dead (Crisp, 1964). Periods of frost may also kill juvenile Patella vulgata, resulting in recruitment failures in some years (Bowman & Lewis, 1977).
The distribution of Patella vulgata is 'northern' with their range extending to the Arctic circle. Over their range they are therefore subject to lower temperatures than in the UK, although distributions should be used cautiously as an indicator of thermal tolerance (Southward et al., 1995).
Sensitivity assessment. The presence of Ulva spp. in arctic regions and the freezing tolerances reported by Vermaat & Sand-Jensen (1987) indicate that Ulva spp., would have ‘High’ resistance to decreases in temperature at the acute and chronic benchmarks. The wide temperature tolerance range of Patella vulgata and Littorina saxatilis suggest that the acute and chronic decreases in temperature described by the benchmark would not lead to mortalities.. Based on the characterizing and associated species, this biotope is considered to have ‘High’ resistance and ‘High resilience (by default) to this pressure and is therefore considered to be ‘Not sensitive’. The timing of changes and seasonal weather could result in greater impacts on species. An acute decrease in temperature coinciding with unusually low winter temperatures may exceed thermal tolerances and lead to mortalities of the associated species although this would not alter the character of the biotope.
The biotope typically experiences conditions of full (30-40 psu) or variable (reduced, owing to freshwater runoff) salinity. The key characterizing Ulva species can survive the hypersaline conditions in supralittoral rockpools subjected to evaporation and is considered to be a very euryhaline species, tolerant of extreme salinities ranging from 0 psu to 136 psu (Reed & Russell, 1979). Some variations in salinity tolerance between populations of Ulva intestinalis have been found, however, suggesting that plants have some adaptation to the local salinity regime. Alströem-Rapaport et al., (2010), found that in the brackish Baltic Sea, Ulva intestinalis uses a variety of reproductive modes which was considered to partly explain the high rates of colonisation and adaptability of the species.
Reed & Russell (1979) found that the ability to regenerate from cut thalli varied according to the salinity conditions of the original habitat, and that the pattern of euryhalinity in parental material and offspring was in broad agreement (Reed & Russell (1979). Eulittoral zone material showed decreased percentage regeneration in concentrated seawater: 51, 68, 95, 102 & 136 psu) when compared to littoral fringe populations of Ulva intestinalis (as Enteromorpha intestinalis). Increased salinity is most likely to occur in the region of the littoral fringe and supralittoral zone and specimens from these areas were able to tolerate very high salinities, a significant decrease in regeneration only being recorded after exposure to concentrated seawater (102 psu and 136 psu) for > 7 days (Reed & Russell, 1979).
Sensitivity assessment. The characterizing Ulva species and the associated species are considered able to tolerate increases in salinity. Based on reported distributions and the results of experiments to assess salinity tolerance thresholds and behavioural and physiological responses it is considered that Ulva spp. and the associated littorinids and limpets would tolerate a change in salinity from variable or reduced to full and some salinity increases above full salinity. As the associated species occur only in low numbers and do not characterize the biotope the sensitivity assessment is based on the Ulva species alone. Biotope resistance is assessed as 'High' and resilience as 'High', based on no effect to recover from and the biotope is considered to be 'Not sensitive'.
The biotope typically experiences conditions of full (30-40 psu) or variable (reduced, owing to freshwater runoff) salinity. The key characterizing Ulva species are considered to be a very euryhaline, tolerant of extreme salinities ranging from 0 psu to 136 psu (Reed & Russell, 1979). Some variations in salinity tolerance between populations of Ulva intestinalis have been found, however, suggesting that plants have some adaptation to the local salinity regime. Alströem-Rapaport et al., (2010), found that in the brackish Baltic Sea, Ulva intestinalis uses a variety of reproductive modes which was considered to partly explain the high rates of colonisation and adaptability of the species. Reed & Russell (1979) found that the ability to regenerate from cut thalli varied according to the salinity conditions of the original habitat, and that the pattern of euryhalinity in parental material and offspring was in broad agreement (Reed & Russell (1979). For example; eulittoral zone material showed decreased percentage regeneration in all salinities (dilute: 0, 4.25, 8.5, 17 & 25.5 psu, and concentrated seawater: 51, 68, 95, 102 & 136 psu) except 34 psu, when compared to littoral fringe populations of Ulva intestinalis (as Enteromorpha intestinalis). None of the eulittoral zone material was able to regenerate in freshwater or concentrated seawater, whilst littoral fringe and rock pool material was able to do so.
Reduced salinity has also been reported to affect the growth rate of Ulva intestinalis. Martins et al. (1999) observed that in years with high precipitation and significant increase of freshwater runoff to the Mondego estuary (west Portugal), that Ulva intestinalis (as Enteromorpha intestinalis) failed to bloom. In the laboratory, the growth rate of Ulva intestinalis was measured against a range of salinities, from 0 to 32 psu. Ulva intestinalis showed the lowest growth rates at extremely low salinity values (less than or equal to 3 psu), and for salinity less than or equal to 1 psu, the algae died. Growth rates at a salinity lower than 5 psu and higher than 25 psu were also low, in comparison to growth between a salinity of 15 and 20 psu, where Ulva intestinalis showed the highest growth rates. Kamer & Fong (2001) found that high nitrogen enrichment mitigated the negative effects that reduced salinity had on Ulva intestinalis (as Enteromorpha intestinalis).
Evidence on salinity tolerances was also found for the associated species that occur in low numbers in this biotope. Like other intertidal species these are exposed to changes in salinity resulting from evaporation or run-off and consequently can tolerate changes in salinity. Populations of Patella vulgata extend into the mouths of estuaries surviving in salinities down to about 20psu. However, growth and reproduction may be impaired in reduced salinity. Little et al. (1991), for example, observed reduced levels of activity in limpets after heavy rainfall and in the laboratory activity completely stopped at 12psu although individuals died only when the salinity was reduced to 3-1psu (Fretter & Graham, 1994). In experiments where freshwater was trickled over the shell Arnold (1957) observed limpets withdrawing and clamping the shell onto the substratum. There appears to be an increasing tolerance of low salinities from the lower to the upper limit of distribution of the species on the shore (Fretter & Graham, 1994) suggesting local acclimation. Littorina littorea is found in waters of full, variable and reduced salinities (Connor et al., 2004) and so populations are not likely to be highly intolerant of decreases in salinity. Therefore, it appears that the biotope would have low intolerance to a decrease in salinity. On return to normal conditions recovery is likely to be very rapid.
Sensitivity assessment. The characterizing Ulva species and the associated species Littorina littorea are considered able to tolerate a change from full to variable or variable to reduced salinity. However, based on reported distributions and the results of experiments to assess salinity tolerance thresholds and behavioural and physiological responses in Patella vulgata it is considered that these species would tolerate a change in salinity from full to variable but that a change from variable to reduced salinity may reduce habitat suitability. As these species occur only in low numbers and do not characterize the biotope the sensitivity assessment is based on the Ulva species alone. Biotope resistance is therefore assessed as 'High' and resilience as 'High', based on no effect to recover from and the biotope is considered to be 'Not sensitive'.
The key characterizing species of this biotope, Ulva intestinalis and Ulva lactuca are flexible and conform to the direction of the flow reducing drag and breakage. However, experimental studies show that exposure to currents results in sloughing of tissue and higher current velocities result in breakage of the thallus.
Kennison & Fong (2013) found that Ulva intestinalis, settled on ceramic tiles and deployed in the field were subject to greater losses at mean flow speeds of 0.2 m/s (approximately 16% of biomass) than the 8% loss from individuals subject to lower flows (0.15 m/s). These results agree with those from another study by Flindt et al. (2007) that subjected Ulva spp. to increased water flows in flume tanks. They distinguished Ulva sp. and Enteromorpha sp. in their sloughing experiments but not to species level. Water flow rates were increased from still incrementally by 0.005 m/s and the amount of biomass sloughed off was measured. At a current speed of 0.12 m/s, 3-4% of biomass of Ulva sp. was removed, increasing to 4-7% at 0.15 m/s and 40-50% at 0.4 m/s. Enteromorpha sp. were slightly more resistant; at current flows of 0.2 m/s 1% of biomass was sloughed, increasing to 20% at 0.35 m/s. Flindt et al., (2007) estimated from regression models that the current speeds at which all Ulva spp., would be totally removed were 0.82 m/s and 1.28 m/s for Enteromorpha sp. Note, Enteromorpha is now a synonym of Ulva. The authors assume that the Enteromorpha sp. mentioned in their study relate to the more filamentous and tube-like growth form of Ulva intestinalis.
Modelled predictions of thallus breakage based on laboratory studies of Ulva lactuca on bivalve shells estimate that large Ulva lactuca (>50 cm in length) are unlikely to persist where currents exceed 0.5 m/s, whereas smaller individuals (24 cm in length) are unlikely to be present where current speeds exceed 1 m/s (Hawes & Smith, 1995). Increased water flows may also be beneficial where these enhance recruitment. Increased water velocities can enhance recruitment through increased larval supply (Kennison & Fong, 2013). Houghton et al. (1973) observed that swarmers of Ulva were able to settle onto surfaces subjected to water speeds of up to 10.7 knots, suggesting that changes may not inhibit settlement.
Sensitivity assessment. Increased water flow rates may detach and remove biomass of the Ulva spp, that characterize this biotope. Experiments suggest that the pressure benchmark is biologically relevant, i.e. increases at the pressure benchmark could result in loss and detachment. However as this biotope occurs in the upper eulittoral or littoral fringe in rockpools (Connor et al., 2004) it will only be exposed for very limited periods and rapid growth of Ulva sp. may mitigate the loss of tissue during the growing season. The experiments do not detail the amount of time that individuals were exposed to flows so that extrapolating the results to predicted losses, particularly for breakage is problematic. Based on the breakage studies (Hawes & Smith, 1995), resistance of Ulva sp., to an increase in water flow at the pressure benchmark is assessed as ‘Medium’ as smaller individuals can persist at flow rates that are almost double those of larger plants and duration of exposure is limited. Resilience is assessed as ‘High’ and sensitivity is assessed as ‘Low’.
As Ulva intestinalis is able to tolerate dessication stress it is often very abundant on the high shore where desiccation stress is the primary factor controlling seaweed distribution, and may even be found above the tidal limits of the shore. Ulva intestinalis (studied as Enteromorpha 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. However, dessication stress of germlimgs may be lower than adults Hruby & Norton (1979) found that 7-14 day old germlings of Ulva (studied as Enteromorpha) were more tolerant of desiccation than earlier stages, so an increase in desiccation stress, resulting in the rock pool drying out may impact more adversely on newly settled germlings than more mature plants
Increased emergence may reduce habitat suitability for the associated species, although the mobile species present within the biotope, Patella vulgata and the littorinids are able to relocate to preferred shore levels. An increase in emergence may result in migration downshore, while decreased emergence may increase habitat suitability of upper littoral fringe biotopes for these species. Grazing by littornids and other species can have a significant structuring impact on biotopes dominated by ephemeral algae (Robles 1982, Albrecht, 1998). An increase in grazers and grazing within this biotope may removal large amounts of algal biomass preventing blooms.
Sensitivity assessment. As this biotope occurs right at the very top of the shore, a change at the pressure benchmark may result in drying of the pool, an increase in environmental stress through increased exposure to air temperatures, increased or decreased salinity and the risk of the pool drying out. Increased submergence would reduce the effects of environmental stress and as this is a key factor maintaining the biotope this may result in a reduction in suitability, depending on the duration of submergence. Increased grazing by littorinids and other grazers facilitated by increased immersion and salinity would also be likely to reduce the biomass of Ulva spp. in this instance. Resistance is assessed as ‘Low’ to both an increase and decrease in emergence and resilience as ‘High’ (following habitat recovery). Sensitivity is therefore assessed as ‘Low’.
The effects of wave exposure upon rockpool communities high on the shore are likely to depend on tidal amplitude as within a shore, and where the tidal amplitude is significant, the time for which organisms are subjected to wave action will vary along the intertidal gradient. For instance, during neap tide periods, high shore rockpools may remain isolated from the main body of the sea for several days or weeks in concession. During such times wave action is unlikely to be of direct influence other than generating a spray, whilst during periods of tidal immersion wave action may directly affect the community. No direct evidence was found to assess the sensitivity of this biotope to changes in wave exposure at the pressure benchmark. This biotope is recorded from locations that are judged to range from very exposed, exposed, moderately exposed and sheltered (Connor et al., 2004). The degree of wave exposure influences wave height, as in more exposed areas with a longer fetch waves would be predicted to be higher. As this biotope occurs across three wave exposure categories, this was therefore considered to indicate, by proxy, that biotopes in the middle of the wave exposure range would tolerate either an increase or decrease in significant wave height at the pressure benchmark.
Sensitivity assessment. The natural wave exposure range of this biotope is considered to exceed changes at the pressure benchmark and this biotope is considered to have 'High' resistance and 'High' resilience (by default), to this pressure (at the benchmark).
|Not relevant (NR)||Not relevant (NR)||Not sensitive|
Not sensitive at the pressure benchmark that assumes compliance with all relevant environmental protection standards.
Contamination by non-synthetic chemicals, at levels greater than the pressure benchmark may adversely impact the biotope. The order of metal toxicity to algae varies, with the algal species and experimental conditions, but generally the order is Hg>Cu>Cd>Ag>Pb>Zn (Rice et al., 1973; Rai et al., 1981). The effects of copper on macrophytes have been more extensively studied than the effects of any other metal owing to its use in antifouling paints. Lewis et al. (1998) investigated the influence of copper exposure and heatshock on the physiology and cellular stress response of Ulva intestinalis (as Enteromorpha intestinalis). Heat shock proteins (HSPs) are known to be expressed in response to a variety of stress conditions, including heavy metals (Lewis et al., 1999). Ulva intestinalis was exposed to a range of copper concentrations (0-500 µg -1 for 5 days, to assess the effect of copper exposure on stress proteins (Stress-70 levels) and physiology of the seaweed. Stress-70 was induced by copper exposure, but was found to be no better an indicator of copper exposure than measurement of growth, which is inhibited by copper.
In the Fal estuary Patella vulgata occurs at, or just outside, Restronguet Point at the end of the creek where metal concentrations are in the order: Zinc (Zn) 100-2000µg/l, copper (Cu) 10-100µg/l and cadmium (Cd) 0.25-5µg/l (Bryan & Gibbs, 1983). However, in the laboratory Patella vulgata was found to be intolerant of small changes in environmental concentrations of Cd and Zn by Davies (1992). At concentrations of 10µg/l pedal mucus production and levels of activity were both reduced, indicating a physiological response to metal concentrations. Exposure to Cu at a concentration of 100µg/l for one week resulted in progressive brachycardia (slowing of the heart beat) and the death of limpets. Zn at a concentration of 5500µg/l produced the same effect (Marchan et al.,1999).
|Not relevant (NR)||Not relevant (NR)||Not sensitive|
Not sensitive at the pressure benchmark that assumes compliance with all relevant environmental protection standards.
Hydrocarbon contamination, at levels greater than the benchmark, e.g. from spills of fresh crude oil or petroleum products, may cause significant loss of Ulva spp. 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 in 1967, grazing species were killed, and a dense flush of ephemeral green algae (Ulva, Blidingia) appeared on the rocky shore within a few weeks and persisted for up to one year (Smith, 1968).
|Not relevant (NR)||Not relevant (NR)||Not sensitive|
Not sensitive at the pressure benchmark that assumes compliance with all relevant environmental protection standards.
Contamination at levels greater than the benchmark may impact this biotope. Some evidence for adverse effects of chemical pollution on the key characterizing species, Ulva intestinalis, has been found. Although herbicides tend not to be used directly in the marine environment, they can enter estuarine areas via river discharge and runoff. Paraquat and 3AT were tested for their effects on the settlement, germination and growth of Ulva (as Enteromorpha) (Moss & Woodhead, 1975). They found that zygotes were able to develop into filaments in the presence of Paraquat at 7 mg/L, but that germination was deferred at higher concentrations. Zygotes demonstrated increased resistance when they settled in clumps on the substratum, and green thalli of Ulva were more susceptible than ungerminated zygotes. Ulva was more intolerant of 3AT than to Paraquat (Moss & Woodhead, 1975).
Synthetic chemicals used as antifouling agents may be directly introduced into the marine environment. 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. Irgarol 1051 was detected at all sampling sites within the Sound; the highest levels were found in close proximity to areas of high boat density, especially where water flow was restricted within marinas, although concentrations within the semi-enclosed Sutton Harbour were less than values predicted from leach rate data. The highest detected concentration of over 120 ng/L significantly inhibited the growth of Ulva intestinalis (as Enteromorpha intestinalis) spores under laboratory conditions; the no effect concentration was 22 ng/L. Photosynthetic efficiency in the adult frond of Ulva intestinalis from Sutton Harbour marina was inhibited by Irgarol 1051 in the laboratory with an EC 50 (72 h) of 2.5 µg/L. A small adverse impact on Ulva intestinalis reproduction within harbours is therefore likely.
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 was especially affected, and included Ulva intestinalis (as Enteromorpha intestinalis) in high level rock pools where it was killed (Smith, 1968).Synthetic compound contamination, at levels greater than the benchmark, is likely to have a variety of effects depending the specific nature of the contaminant and the species group(s) affected. Hoare & Hiscock (1974) reported that the limpet Patella vulgata was excluded from sites within 100-150m of the discharge of acidified, halogenated effluent in Amlwch Bay. Limpets are also extremely intolerant of aromatic solvent based dispersants used in oil spill clean-up. During the clean-up response to the Torrey Canyon oil spill nearly all the limpets were killed in areas close to dispersant spraying. Viscous oil will not be readily drawn in under the edge of the shell by ciliary currents in the mantle cavity, whereas detergent, alone or diluted in seawater, would creep in much more readily and be liable to kill the limpet (Smith, 1968). A concentration of 5ppm killed half the limpets tested in 24 hours (Southward & Southward, 1978; Hawkins & Southward, 1992). Acidified seawater affects the motility of Patella vulgata. At a pH of 5.5 motility was reduced whilst submerged but individuals recovered when returned to normal seawater. At a pH of 2.5 total inhibition of movement occurred and when returned to normal seawater half had died (Bonner et al., 1993). Reduced motility reduces time for foraging and may result in decreased survival of individuals. Acidified seawater can also change the shell composition which will lead to a decrease in its protective nature and hence survival (Bonner et al., 1993). Short periods (48 hours) are unlikely to have much effect on a population but long periods (1 year) may cause reduced grazing and an increase in algal growth. However, seawater is unlikely to reach pH 2.5 therefore intolerance to slight changes in pH will be low. Gastropod molluscs are known to be intolerant of endocrine disruption from synthetic chemicals such as tri-butyl tin (Cole et al., 1999). However no information on the specific effects of tri-butyl tin on Patella vulgata was found. Hoare & Hiscock (1974) reported that in Amlwch Bay Patella vulgata was excluded from sites within 100-150 m of the discharge of acidified, halogenated effluent.
The key characterizing Ulva spp. are known to be able to acquire large concentrations of 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). Based on this evidence, the resistance of the biotope to this pressure at the benchmark, is assessed as 'High', resilience is assessed as 'High' (by default), and the biotope is assessed as 'Not sensitive'.
|Not relevant (NR)||Not relevant (NR)||Not sensitive|
Algae produce oxygen by photosynthesis, and this may raise oxygen concentrations in rock pools up to three times the saturation value. At night, when photosynthesis has ceased, algal respiration may utilize much of the available oxygen and minimum values of 1-5 % saturation have been recorded (Morris & Taylor, 1983). Algae in this biotope are therefore unlikely to be adversely affected by decreased oxygen as they re-oxygenate the rock pool. The evidence for anoxia tolerances have, however been reviewed.
Where nutrients and other factors support rapid growth, large blooms of Cladophora spp. and Ulva spp. can occur, as these die and decay, they can create anoxic conditions in the water column and the sediments they overlay. Some tolerance for anoxia may therefore be expected that allows a proportion of the population to survive and reproduce during and after these conditions. Vermaat & Sand-Jensen (1987) tested the survival of discs of Ulva lactuca during prolonged exposure to anoxia. The 113 mm2 discs were taken from wild plants collected in the Roskilde Fjord, Denmark in late autumn. Anoxic conditions were created in the laboratory by bubbling with N2 gas. Exposure to anoxia for two months did not affect survival but did result in increased respiration and a decrease in growth. Corradi et al., (2006) used similar sized thallus discs from Ulva spp. (113 mm 2), collected from the lagoon Sacca di Goro (Po River Delta) during spring to test the effects of hypoxia on gamete production for Ulva sp. The test oxygen concentrations ranged from 1.78 – 4.02 µmol /L (the benchmark of 2mg/l refers to 64 µmol/L). The exposure to hypoxia was not lethal to the discs and following resumption of normal oxygen conditions gametes were produced.
The associated species also show high tolerances for reduced oxygen. The effect of severe hypoxia on the copepod Tigriopus brevicornis is for it to enter a quiescent/dormant state during which its metabolic rate is significantly reduced. It recovers on return to optimal conditions (McAllen et al., 1999). Littorina littorea also have a high tolerance for low oxygen conditions and can easily survive 3-6 days of anoxia (Storey et al., 2013). In laboratory experiments a reduction in the oxygen tension of seawater from 148mm Hg (air saturated seawater) to 50mm Hg rapidly resulted in reduced heart rate in limpets of the genus Patella (Marshall & McQuaid, 1993). Heartbeat rate returned to normal in oxygenated water within two hours. Limpets can survive for a short time in anoxic seawater; Grenon & Walker, (1981) found that in oxygen free water limpets could survive up to 36 hours, although Marshall & McQuaid (1989) found a lower tolerance for Patella granularis, which survived up to 11 hours in anoxic water. It should be noted that the mobile littorinids and Patella vulgata would be able to leave a deoxygenated rockpool and can breathe air.
Sensitivity assessment. No direct evidence for the effects of hypoxia on whole plants in-situ was available. However the results of the laboratory experiments which tested parts of Ulva individuals to either prolonged anoxia or short-term hypoxia at levels that exceed the benchmark, indicate that Ulva have ‘High’ resistance to this pressure and ‘High’ resilience by default. The associated species, littorinids and Patella vulgata are considered to be ‘Not Sensitive’ to de-oxygenation at the pressure benchmark. The experiments cited as evidence (Grenon & Walker, 1981 and Barnes et al.,1963) exceed the duration and/or magnitude of the pressure benchmark. Biotope resistance is therefore assessed as ‘High’ and resilience as ‘High’ (no effect to recover from), resulting in a sensitivity of 'Not sensitive'.
This pressure relates to increased levels of nitrogen, phosphorus and silicon in the marine environment compared to background concentrations. The pressure benchmark is set at compliance with Water Framework Directive (WFD) criteria for good status, based on nitrogen concentration (UKTAG, 2014).
The criteria for status under the WFD with regard to nutrient enrichment is concerned with the presence or absence of ‘blooms’ of opportunistic algae , including the key characterizing Cladophora spp. and Ulva spp. found in this biotope, that act as indicators of enrichment (eutrophication). The abundance and biomass of these species are used in the implementation of the WFD as indicators to assess the condition of waterbodies. The criteria for achieving good status states that there should be: ‘limited cover (<15%) and low biomass (<500g/m2) of opportunistic macroalgal blooms…macroalgae cover shows slight signs of disturbance with a slight deviation from reference conditions’ (Wells et al., 2014).
The high abundance and biomass of Ulva spp, that characterize this biotope would suggest that this biotope would fail to achieve ‘good status’. Theoretically, compliance with good status would require a significant loss of characterizing species, suggesting that the biotope would be sensitive to this pressure at the benchmark (i.e. it represents a significant impact on biotope character). However, the biotope is considered to develop in response to chronic stressors in tide pools high on the shore. Typical blooms of opportunistic macroalgae, occur in sheltered areas such as estuaries (Kennison & Fong, 2013) and are likely to form as unattached mats over sediments rather than rocky shores, the character of these is therefore different to the assessed biotope.
Opportunistic algae, including Ulva spp. cannot store nutrients in the thallus (unlike larger, long-lived species) and are adapted to efficiently capture and utilise available nutrients in the water column (Pedersen et al., 2009). A large body of field observations and experiments, surveys and laboratory experiments confirm that the characterizing Ulva spp, can utilise high levels of nutrients for growth (Martínez et al., 2012) and that enhanced recruitment (Kraufvelin, 2007) and growth of this genus can occur in enriched areas (Kennison & Fong, 2013, Vaudrey et al., 2010). Such as Ulva sp. in the Lagoon of Venice (Sfriso et al. 1987) and Cladophora sp. in Laholm Bay, Sweden(Baden et al. 1990). In areas where nutrient availability is lower either naturally or through management to reduce anthropogenic inputs, Ulva spp. may be negatively affected through reduced growth rate and species replacement (Martínez et al., 2012; Vaudrey et al., 2010).
The associated species Littorina littorea occurs on all British and Irish coasts, including lower salinity areas such as this estuarine biotope where nutrient loading is likely to be higher than elsewhere. Higher nutrient levels may benefit the algal substrata and food used by the snail. In situations with nutrient enrichment, primary productivity in terms of biofilms and/ or green algae will generally be enhanced, which may supply more food or more nutrient rich food. This can reduce the browsing distances and periods of Littorina, reducing times spent searching for food (Diaz et al. 2012). After five months of nutrient addition in experimental mesocosms, Littorina abundance and biomass had increased compared to controls. Enriched mesocosms experiments were treated with 32 lM inorganic nitrogen (N) and 2 lM inorganic phosphorus (P) above the background levels in the Oslofjord continuously in the period April–September 2008. These nutrient addition levels are similar to concentrations recorded in eutrophic areas locally (Kristiansen & Paasche, 1982; cited in Diaz et al. 2012) and globally (Cloern, 2001; cited in Diaz et al. 2012).
Sensitivity assessment. If nutrient levels were to increase (exceeding the pressure benchmark) enhanced growth of Cladophora spp. and Ulva spp. would be expected in response and this is not considered to significantly alter the character of the biotope. Cladophora and Ulva spp. may decline in response to reductions in nutrient levels, in habitats where other species more typical of undisturbed species are able to recolonize. However, as this biotope is structured by salinity variations and other environmental stressors rather than nutrient enrichment, other species are not considered to establish following decreases in nutrient levels and Cladophora and Ulva spp, would be likely to remain the dominant species. The biotope is therefore considered to have ‘High’ resistance to this pressure and ‘High’ resilience, (by default) and is assessed as ‘Not sensitive’.
Organic enrichment may lead to eutrophication with adverse environmental effects including deoxygenation, algal blooms and changes in community structure (see nutrient enrichment and de-oxygenation). Little evidence was found to support this assessment, Cabral-Oliveira et al., (2014), found higher abundances of juvenile Patella sp. and lower abundances of adults closer to sewage inputs, Cabral-Oliveira et al., (2014) suggested the structure of these populations was due to increased competition closer to the sewage outfalls.
Sensitivity assessment. No empirical evidence was found to support an assessment for the key characterizing Ulva spp., or the associated species that are present within this biotope. As organic matter particles in suspension or re-suspended could potentially be utilised as a food resource by filter feeders with excess likely to be rapidly removed by wave action, overall resistance of the biological assemblage within the biotope is considered to be 'High' and resilience was assessed as 'High', so that this biotope is judged to be 'Not sensitive'.
All marine habitats and benthic species are considered to have a resistance of ‘None’ to this pressure and to be unable to recover from a permanent loss of habitat (resilience is ‘Very Low’). Sensitivity within the direct spatial footprint of this pressure is therefore ‘High’. Although no specific evidence is described confidence in this assessment is ‘High’, due to the incontrovertible nature of this pressure.
This biotope occurs in tidepools on hard substrata where the key characterizing Ulva and Cladophora spp. can attach to the rock. A soft sedimentary habitat would not retain water and would be unsuitable for these species and the associated species Patella vulgata (although littorinids occur on sediment). A change to a soft sedimentary biotope would lead to the development of a biological assemblage more typical of the changed conditions.
Sensitivity assessment. A change to a sedimentary habitat would remove this biotope, resistance is assessed as ‘None’ and resilience as ‘Very Low’ as the change is considered to be permanent. Sensitivity is therefore assessed as 'High'.
|Not relevant (NR)||Not relevant (NR)||Not relevant (NR)|
Not relevant to this biotope which occurs in tidepools on bedrock (Connor et al., 2004).
|Not relevant (NR)||Not relevant (NR)||Not relevant (NR)|
The key characterizing Ulva and Cladophora spp. and associated species are epifauna or epiflora occurring on rock in tidepools and would be sensitive to the removal of the habitat. However, extraction of rock substratum is considered unlikely and this pressure is considered to be ‘Not relevant’ to hard substratum habitats.
No direct evidence was found to assess how the key, characterizing, Cladophora and Ulva spp. respond to surface abrasion. Ulva spp. fronds are very thin and could be torn and damaged and individuals may be removed from the substratum, altering the biotope through changes in abundance and biomass. Ulva spp. cannot repair damage or reattach but torn fronds could still photosynthesise and produce gametes. Tearing and cutting of the fronds has been shown to stimulate gamete production and damaged plants would still be able to grow and reproduce. Ulva spp. can also form unattached mats (particularly in response to nutrient enrichment): damage and removal may, therefore, not lead to mortality of impacted individuals. Cladophora spp. have a relatively tough thallus (Dodds & Gudder, 1992) but no direct evidence was found for resistance to abrasion. In Kimmeridge Bay in Southern England, Pinn & Rodgers (2005) found that the abundance of Cladophora rupestris was lower at a more heavily visited and trampled site.
The limpets and littorinids that occur in low densities in this biotope, have some protection from hard shells but abrasion may damage and kill individuals or detach them from suitable habitats. All removed barnacles would be expected to die as there is no mechanism for these to reattach. Removal of limpets may result in these being displaced to a less favourable habitat and injuries to foot muscles in limpets may prevent reattachment. Although limpets and littorinids may be able to repair shell damage, broken shells while healing will expose the individual to more risk of desiccation and predation. Evidence for the effects of abrasion are provided by a number of experimental studies on trampling (a source of abrasion) and on abrasion by wave thrown rocks and pebbles.
Povey & Keough (1991) in experiments on shores in Mornington peninsula, Victora, Australia, found that limpets may be relatively more resistant to abrasion from trampling. Following step and kicking experiments, few individuals of the limpet Cellana trasomerica, (similar size to Patella vulgata) suffered damage or relocated (Povey & Keough, 1991). One kicked limpet (out of 80) was broken and 2 (out of 80) limpets that were stepped on could not be relocated the following day (Povey & Keough, 1991). On the same shore less than 5% of littorinids were crushed in single step experiments (Povey & Keough, 1991).
Shanks & Wright (1986), found that even small pebbles (<6 cm) that were thrown by wave action in Southern California shores could smash owl limpets (Lottia gigantea). Average, estimated survivorship of limpets at a wave exposed site, with many loose cobbles and pebbles allowing greater levels of abrasion was 40% lower than at a sheltered site. Severe storms were observed to lead to almost total destruction of local populations of limpets through abrasion by large rocks and boulders. In sites with mobile cobbles and boulders increased scour results in lower densities of Littorina spp. compared with other, local sites with stable substratum (Carlson et al., 2006).
Sensitivity assessment. The impact of surface abrasion will depend on the footprint, duration and magnitude of the pressure. In response to a single event of abrasion a proportion of the Cladophora spp. and Ulva population may be removed, but damaged individuals, in-situ would be capable of growth and reproduction. Based on additional evidence for the associated species from the step experiments and the relative robustness of the associated species, the resistance of the biotope, to a single abrasion event is assessed as ‘Medium’ and recovery as ‘High’, so that sensitivity is assessed as ‘Low’. Resistance will be lower (and hence sensitivity greater) to abrasion events that exert a greater crushing force than the trampling examples the assessment is based on).
|Not relevant (NR)||Not relevant (NR)||Not relevant (NR)|
The species characterizing this biotope group are epifauna or epiflora occurring in tidepools on rock which is resistant to subsurface penetration. The assessment for abrasion at the surface only is therefore considered to equally represent sensitivity to this pressure.
Intertidal biotopes will only be exposed to this pressure when submerged during the tidal cycle and thus have limited exposure. Siltation, which may be associated with increased suspended solids is assessed separately. As a photoautotroph, the key characterizing Ulva spp., are likely to benefit from reduced turbidity, as the light attenuating effects of turbid water reduce photosynthesis. However experiments have shown that Ulva is a shade tolerant species and can compensate for reduced irradiance by increasing chlorophyll concentration and light absorption at low light levels. Ulva spp. were able to survive over two months in darkness and to begin photosynthesising immediately when returned to the light (Vermaat & Sand-Jensen, 1987). Limited shading from suspended sediments is therefore not considered to negatively affect this genus. Suspended sediments may however have abrading effects on the fronds of Ulva spp. Tolhurst et al. (2007) found that Ulva intestinalis germlings kept in tanks and exposed to 100 mg/l of suspended sediment showed reduced growth. Similarly, Hyslop & Davies (1998) found that Ulva lactuca lost weight when kept in flasks with 1 g/l of colliery waste that was shaken for 1 hour every day for 8 days. The experimental solids level, however, exceeds the pressure benchmark and oscillatory flows will be limited to periods where he rockpool is inundated by the tide and exposed to waves. It should be noted that both Cladophora spp. and Ulva spp. can occur in estuaries and/or eutrophicated areas where levels of suspended solids can be very high.
Sensitivity assessment. The exposure of this upper shore biotope to suspended sediments in the water column will be limited to the short immersion periods, however silts deposited during emersion may remain on the fronds inhibiting photosynthesis in sheltered areas. The biotope is considered to be ‘Not sensitive’ to a reduction in suspended solids. An increase in suspended solids from clear (<10 mg/l) to intermediate (10-100 mg/l) may lead to some sub-lethal abrasion of fronds and reduction in photosynthesis but this will be compensated by the high growth rates exhibited by Cladophora and Ulva spp. Resistance is therefore assessed as ‘High’ and resilience as ‘High’ (by default) so that the biotope is considered to be ‘Not sensitive’.
Observations and experiments indicate that Ulva spp. have relatively high tolerances for the stresses induced by burial (darkness, hypoxia and exposure to sulphides). Vermaat & Sand-Jensen , (1987) exposed thallus discs (113 mm2) of Ulva lactuca to darkness and anoxia and sulphides at winter temperatures. It was found that these conditions did not affect survival over two months, although exposure to anoxia increased respiration and reduced growth (Vermaat & Sand-Jensen, 1987). These experiments were undertaken using Ulva lactuca collected from Roskilde Fjord, Denmark. Corradi et al., (2006) subjected Ulva sp. collected from the Sacca di Goro, Italy to similar stressors (hypoxia 1.78 – 4.02 µmol /L, or sulphide at 1mM, both treatments in darkness) for 3,5 or 7days at 20oC. The thallus discs survived but no gametes were produced until recovery in oxygenated conditions. The high tolerance of darkness, anoxia and hydrogen sulphides allows buried fragments of Ulva sp. to overwinter, protected from frosts. Kamermans et al., (1998) found that parts of Ulva thalli that were collected from the Veerse Meer lagoon in the Netherlands could resume growth in the spring when returned to the surface. Ulva spp. in sheltered areas are often unattached to the substratum and therefore are not considered a direct proxy for attached Ulva spp. in this biotope.
Although Ulva spp. present in sedimentary habitats may be able to survive the chemical stress of burial and re-grow from surviving fragments, evidence for attached individuals from rocky shores suggest that resistance to this pressure may be lower. Ulva lactuca is a dominant species on sand-affected rocky shores in New Hampshire (Daly & Mathieson, 1977) although Littler et al., (1983) suggest that Ulva sp., are present in areas periodically subject to sand deposition not because they are able to withstand burial but because they are able to rapidly colonise sand-scoured areas (such as this biotope). Ulva spp. have, however, been reported to form turfs that trap sediments (Airoldi, 2003, references therein) suggesting that resistance to chronic rather than acute siltation events may be higher. In general, propagules, early post-settlement stages and juveniles suffer severe stress and mortality from sediments (Airoldi, 2003). Hyslop et al. (1997) compared the composition, abundance and distribution of dominant plants and animals at several rocky shores affected or unaffected by dumping of colliery wastes along the coastline of northeast England. They reported that while the distribution of animals was not related to colliery wastes, diversity of macroalgae was significantly negatively correlated with colliery waste inputs and particularly dramatic reductions in cover at the affected sites were observed for Ulva lactuca. The authors suggested that, because colliery waste leaches much of its toxic chemical content into the sea, detrimental effects were most likely related to the physical presence of sediments.
The associated species, Patella vulgata and Littorina spp. are likely to be negatively affected by siltation. Experiments have shown that the addition of even thin layers of sediment (approximately 4 mm) inhibit grazing and result in loss of attachment and death after a few days Airoldi & Hawkins (2007). The laboratory experiments are supported by observations on exposed and sheltered shores with patches of sediment around Plymouth in the south west of England as Patella vulgata abundances were higher where deposits were absent (Airoldi & Hawkins (2007). Littler et al., (1983) found that the another limpet species, Lottia gigantea on southern Californian shores was restricted to refuges from sand burial on shores subject to periodic inundation by sands. Chandrasekara & Frid (1998) specifically tested the siltation tolerance of Littorina littorea. Burial to 5cm caused mortality within 24 hours at simulated summer and winter temperatures if the snails could not crawl out of the sediment (Chandrasekara & Frid, 1998). If the sediment is well oxygenated and fluid (as with high water, high silt content) a few snails (1-6 out of 15 in the experiment, depending on temperature, sediment and water content) may be able to move back up through 5 cm of sediment (Chandrasekara & Frid, 1998). Approximately half of the test individuals could not regain the surface from 1cm of burial except in the most favourable conditions (low temperatures, high water, high silt when a majority (10 out of 15) of the test cohort surfaced. Field observations support the findings that Littorina littorea are generally unable to survive smothering. Albrecht & Reise (1994) observed a population of Littorina littorea in a sandy bay near the Sylt island in the North Sea. They found that the accretion of mud within Fucus strands and subsequent covering of Littorina by the sediment resulted in them suffocating and a significant reduction in their abundance.
Sensitivity assessment. A covering of sediment to a depth of 5 cm is likely to partially cover erect Cladophora spp. and may fully cover the flexible Ulva spp. Unless the sediment is removed by the incoming tide (which may be some time on the high shore where pools may be isolated from the main body of the sea for several days in succession), photosynthesis would be inhibited and fronds of macroalgae may begin to decay. If shallow the pool itself may be infilled. The available evidence indicates that Ulva spp. can survive some of the stressors associated with burial but would be sensitive to abrasion and scouring forces resulting from the deposition and removal of sediments. Spores, germlings and juveniles are likely to be highly intolerant of smothering by sediment (Vadas et al. 1992).. Even small deposits of sediments are likely to result in local removal of limpets and littorinids and these are considered to have ‘Low’ resistance to this pressure based primarily on observations and experiments of Airoldi & Hawkins, (2007). The sensitivity assessment for the biotope is based on Ulva and Cladophora spp. Within pools siltation by 5 cm of fine sediments is considered likely to remove a proportion of the population through scour effects and resistance is assessed as ‘Low-Medium’, recovery is assessed as ‘High’ (following removal of silts) and sensitivity is assessed as ‘Low’.
Observations and experiments indicate that Ulva spp. have relatively high tolerances for the stresses induced by burial (darkness, hypoxia and exposure to sulphides). Vermaat & Sand-Jensen (1987) exposed thallus discs (113 mm2) of Ulva lactuca to darkness and anoxia and sulphides at winter temperatures. It was found that these conditions did not affect survival over two months, although exposure to anoxia increased respiration and reduced growth (Vermaat & Sand-Jensen, 1987). These experiments were undertaken using Ulva lactuca collected from Roskilde Fjord, Denmark. Corradi et al., (2006) subjected Ulva sp. collected from the Sacca di Goro, Italy to similar stressors (hypoxia 1.78 – 4.02 µmol /L, or sulphide at 1mM, both treatments in darkness) for 3, 5 or 7days at 20oC. The thallus discs survived but no gametes were produced until recovery in oxygenated conditions. The high tolerance of darkness, anoxia and hydrogen sulphides allows buried fragments of Ulva sp. to overwinter, protected from frosts. Kamermans et al., (1998) found that parts of Ulva thalli that were collected from the Veerse Meer lagoon in the Netherlands could resume growth in the spring when returned to the surface. Ulva spp. in sheltered areas are often unattached to the substratum and therefore are not considered a direct proxy for attached Ulva spp. in this biotope.
Although Ulva spp. present in sedimentary habitats may be able to survive the chemical stress of burial and re-grow from surviving fragments, evidence for attached individuals from rocky shores suggest that resistance to this pressure may be lower. Ulva lactuca is a dominant species on sand-affected rocky shores in New Hampshire (Daly & Mathieson, 1977), although Littler et al., (1983) suggest that Ulva sp., are present in areas periodically subject to sand deposition not because they are able to withstand burial but because they are able to rapidly colonise sand-scoured areas (such as this biotope). Ulva spp. have, however, been reported to form turfs that trap sediments (Airoldi, 2003, references therein) suggesting that resistance to low-level chronic rather than acute siltation events may be higher. In general, propagules, early post-settlement stages and juveniles suffer severe stress and mortality from sediments (Airoldi, 2003). Hyslop et al. (1997) compared the composition, abundance and distribution of dominant plants and animals at several rocky shores affected or unaffected by dumping of colliery wastes along the coastline of northeast England. They reported that while the distribution of animals was not related to colliery wastes, diversity of macroalgae was significantly negatively correlated with colliery waste inputs and particularly dramatic reductions in cover at the affected sites were observed for Ulva lactuca. The authors suggested that, because colliery waste leaches much of its toxic chemical content into the sea, detrimental effects were most likely related to the physical presence of sediments.
The associated species are likely to be negatively affected by siltation as outlined above for the ‘Light’ siltation pressure and no or very few, impacted individuals would be predicted to survive.
Sensitivity assessment. The available evidence indicates that Ulva spp. can survive some of the stressors associated with burial but would be sensitive to abrasion and scouring forces resulting from the deposition and removal of sediments. Even small deposits of sediments are likely to result in local removal of limpets and limpets are considered to have ‘No’ resistance to this pressure based primarily on observations and experiments of Airoldi & Hawkins, (2007) and Chandrasekara & Frid, 1998). The sensitivity assessment for the biotope is based on Ulva spp. Siltation by 30 cm of fine sediments is considered to remove a proportion of the population through scour effects and resistance is assessed as ‘Low’, recovery is assessed as ‘High’ (following removal of silts) and sensitivity is assessed as ‘Low’.
|Not Assessed (NA)||Not assessed (NA)||Not assessed (NA)|
|No evidence (NEv)||No evidence (NEv)||No evidence (NEv)|
|Not relevant (NR)||Not relevant (NR)||Not relevant (NR)|
A number of experiments have demonstrated that the key characterizing species Ulva lactuca, has high tolerance for shading and can survive periods of darkness. Vermaat & Sand-Jensen (1987) found that Ulva lactuca, collected from Roskilde Fjord in Denmark in late autumn had extremely high shade tolerances. Increasing chlorophyll concentration and light absorption allowed the individuals (studied experimentally as thallus discs of 113 mm2) to continue to grow at the lowest irradiance tested (0.6 µE m2/s). This corresponds to the lowest light-levels of deep-living marine macroalgae and phytoplankton growing under ice (Vermaat & Sand-Jensen, 1987). Ulva lactuca was able to survive two months in darkness and was able to resume growth immediately when transferred to the light (Vermaat & Sand-Jensen, 1987).
No direct evidence to assess this pressure was found for the key characterizing species Patella vulgata and the littorinids. As both species occur on open rock and in crevices and under Fucus canopies they are considered tolerant of a range of light conditions.
Sensitivity assessment. The key Ulva spp. that characterizes the biotope are considered to have ‘High’ resistance to changes in light level, although extreme changes such as complete darkness would prevent photosynthesis and growth and high light levels may be damaging. Recovery is assessed as ‘High’ by default and the biotope is judged to be ‘Not sensitive ‘.
No direct evidence was found to assess this pressure. The key characterizing Ulva and Cladophora spp. produce large amounts of motile swarmers, throughout the growing season (Niesenbaum, 1988) . The level of supply of potential recruits is considered to be so great that barriers and changes in tidal excursion will not negatively impact populations. The associated species Patella vulgata and Littorina littorea also produce planktonic larvae that are transported by water movements.. Barriers that reduce the degree of tidal excursion may alter larval supply to suitable habitats from source populations. Conversely the presence of barriers may enhance local population supply by preventing the loss of larvae from enclosed habitats. Littorina saxatilis have either limited dispersal or produce crawl away juveniles rather than pelagic larvae (direct development). Barriers and changes in tidal excursion are not considered relevant to these species as dispersal is limited. As the key characterizing species are widely distributed and have larvae capable of long distance transport, resistance to this pressure is assessed as 'High' and resilience as 'High' by default. This biotope is therefore considered to be 'Not sensitive'.
|Not relevant (NR)||Not relevant (NR)||Not relevant (NR)|
Not relevant to seabed habitats. NB. Collision by grounding vessels is addressed under ‘surface abrasion’.
|Not relevant (NR)||Not relevant (NR)||Not relevant (NR)|
The key characterizing Cladophora and Ulva spp. may be cultivated for use as biofilters to mitigate pollution, as biomass for biofuel generation or for pharmaceuticals and food. No information was found on current production in the UK and no evidence was found for the effects of gene flow between cultivated species and wild populations. As wild populations are widely distributed and water flow may aid dispersal of swarmers, populations are not considered to be genetically isolated. It is therefore considered that resistance to changes in genetic structure are ‘High’ and that resilience is therefore ‘High’ by default and the biotope is ‘Not sensitive’. The use of genetically modified organisms in the future, which may transfer novel genetic material to wild populations may result in harmful impacts and this assessment would require updating if such scenarios arise.
This biotope occurs where either fresh-water influences or physical disturbances, such as abrasion, prevent the development of a more diverse rocky shore assemblage. Due to the environmental stressors that maintain the biotope the habitat is unsuitable for colonisation by most species including invasive, non-indigenous species.
Sensitivity assessment. Based on the high-levels of environmental stress and the lack of habitat overlap and reported impacts with currently recognised invasive, non-indigenous species, this biotope is considered to have ‘High’ resistance and ‘High’ resilience to this pressure and is therefore assessed as ‘Not sensitive’.
No evidence was found that outbreaks of microbial pathogens significantly impact populations of the key characterizing Cladophora and Ulva spp. Resistance to this pressure is therefore assessed as ‘High’ and recovery as ‘High’ (by default) so that the biotope is considered to be ‘Not sensitive’
The winkle Littorina littorea and the limpet Patella vulgata occur in low densities in this biotope and may be gathered by hand. However, as these are not key characterizing species the biotope is not considered sensitive to their removal or the reduction in grazing pressure that may result. The key characterizing Ulva spp. may be collected from the wild for use in pharmaceuticals and food. Removal of this species in high quantities would alter the character of the biotope, resulting in reclassification. Resistance to harvesting is assessed as ‘Low’ as the genus, is relatively large, attached and accessible and therefore has no escape or other avoidance mechanisms. Resilience is assessed as ‘High’ as cleared areas will be readily colonised. Sensitivity is therefore assessed as ‘Low’.
Incidental removal of the characterizing Ulva and Cladophora spp.would alter the character of the biotope. The ecological services such as primary production provided by these species would also be lost.
Sensitivity assessment. Removal of a large percentage of the characterizing species would alter the character of the biotope, so that it was a bare rock pool. Resistance is therefore assessed as ‘Low’ and recovery as ‘High’ and sensitivity is therefore assessed as 'Low'.
Abou-Aisha, K.M., Kobbia, I., El Abyad, M., Shabana, E.F. & Schanz, F., 1995. Impact of phosphorus loadings on macro-algal communities in the Red Sea coast of Egypt. Water, Air, and Soil Pollution, 83 (3-4), 285-297.
Airoldi, L., 2003. The effects of sedimentation on rocky coast assemblages. Oceanography and Marine Biology: An Annual Review, 41,161-236
Airoldi, L. & Hawkins, S.J., 2007. Negative effects of sediment deposition on grazing activity and survival of the limpet Patella vulgata. Marine Ecology Progress Series, 332, 235-240.
Albrecht, A. & Reise, K., 1994. Effects of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgoländer Meeresuntersuchungen, 48 (2-3), 243-256.
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 Ecology, 229 (1), 85-109.
Alströem-Rapaport, C., Leskinen, E. & Pamilo, P., 2010. Seasonal variation in the mode of reproduction of Ulva intestinalis in a brackish water environment. Aquatic Botany, 93 (4), 244-249.
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.
Archer, A.A., 1963. A new approach to the taxonomy of the branched members of the Cladophoraceae in the British Isles. , Ph.D. thesis, Liverpool University.
Arnold, D.C., 1957. The response of the limpet, Patella vulgata L., to waters of different salinities. Journal of the Marine Biological Association of the United Kingdom, 36, 121-128.
Baden, S.P., Pihl, L. & Rosenberg, R., 1990. Effects of oxygen depletion on the ecology, blood physiology and fishery of the Norway lobster Nephrops norvegicus. Marine Ecology Progress Series, 67, 141-155.
Baeck, S., Lehvo, A. & Blomster, J., 2000. Mass occurrence of unattached Enteromorpha intestinalis on the Finnish Baltic Sea coast. Annales Botanici Fennici, 37, 155-161.
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.
Bonner, T. M., Pyatt, F. B. & Storey, D. M., 1993. Studies on the motility of the limpet Patella vulgata in acidified sea-water. International Journal of Environmental Studies, 43, 313-320.
Bowman, R.S., 1985. The biology of the limpet Patella vulgata L. in the British Isles: spawning time as a factor determining recruitment sucess. In The Ecology of Rocky Coasts: essays presented to J.R. Lewis, D.Sc., (ed. P.G. Moore & R. Seed), Hodder and Stoughton, London, pages 178-193.
Bowman, R.S. and Lewis, J.R., 1986. Geographical variation in the breeding cycles and recruitment of Patella spp. Hydrobiologia, 142, 41-56.
Bowman, R.S. & Lewis, J.R., 1977. Annual fluctuations in the recruitment of Patella vulgata L. Journal of the Marine Biological Association of the United Kingdom, 57, 793-815.
Bryan, G.W. & Gibbs, P.E., 1983. Heavy metals from the Fal estuary, Cornwall: a study of long-term contamination by mining waste and its effects on estuarine organisms. Plymouth: Marine Biological Association of the United Kingdom. [Occasional Publication, no. 2.]
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.
Burrows, E.M., 1959. Growth form and environment in Enteromorpha. Botanical Journal of the Linnean Society, 56, 204-206.
Burrows, E.M., 1991. Seaweeds of the British Isles. Volume 2. Chlorophyta. London: British Museum (Natural History).
Cabral-Oliveira, J., Mendes, S., Maranhão, P. & Pardal, M., 2014. Effects of sewage pollution on the structure of rocky shore macroinvertebrate assemblages. Hydrobiologia, 726 (1), 271-283.
Cambridge, M., Breeman, A.M., van Oosterwijk, R. & van den Hoek, C., 1984. Temperature responses of some North American Cladophora species (Chlorophyceae) in relation to their geographic distribution. Helgoländer Wissenschaftliche Meeresuntersuchungen, 38, 349-363.
Carlson, R.L., Shulman, M.J. & Ellis, J.C., 2006. Factors Contributing to Spatial Heterogeneity in the Abundance of the Common Periwinkle Littorina Littorea (L.). Journal of Molluscan Studies, 72 (2), 149-156.
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.
Christie , A.O. & Evans, L.V., 1962. Periodicity in the liberation of gametes and zoospores of Enteromorpha intestinalis Link. Nature, 193, 193-194.
Clark, M.E., 1968. The ecology of supralittoral rockpools with special reference to the copepod fauna. , Ph.D. Thesis, University of Aberdeen, Scotland.
Clark, R.B., 1992. Marine pollution, 3rd edition. Oxford: Clarendon Press.
Clark, R.B., 1997. Marine Pollution, 4th ed. Oxford: Carendon Press.
Cole, S., Codling, I.D., Parr, W., Zabel, T., 1999. Guidelines for managing water quality impacts within UK European marine sites [On-line]. UK Marine SACs Project. [Cited 26/01/16]. Available from: http://www.ukmarinesac.org.uk/pdfs/water_quality.pdf
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.
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.
Corradi, M.G., Gorbi, G. & Zanni, C., 2006. Hypoxia and sulphide influence gamete production in Ulva sp. Aquatic Botany, 84 (2), 144-150.
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.
Cullinane, J.P., McCarthy, P. & Fletcher, A., 1975. The effect of oil pollution in Bantry Bay. Marine Pollution Bulletin, 6, 173-176.
Daly, M.A. & Mathieson, A.C., 1977. The effects of sand movement on intertidal seaweeds and selected invertebrates at Bound Rock, New Hampshire, USA. Marine Biology, 43, 45-55.
Davenport, J. & Davenport, J.L., 2005. Effects of shore height, wave exposure and geographical distance on thermal niche width of intertidal fauna. Marine Ecology Progress Series, 292, 41-50.
Davenport, J., Barnett, P.R.O. & McAllen, R.J., 1997. Environmental tolerances of three species of the harpacticoid copepod genus Tigriopus. Journal of the Marine Biological Association of the United Kingdom, 77, 3-16.
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.
Davies, M.S., 1992. Heavy metals in seawater: effects on limpet pedal mucus production. Water Research, 26, 1691-1693.
Davies, S.P., 1970. Physiological ecology of Patella IV. Environmental and limpet body temperatures. Journal of the Marine Biological Association of the United Kingdom, 50 (04), 1069-1077.
Dethier, M.N., 1980. Tidepools as refuges: predation and the limits of the harpacticoid copepod Tigriopus californicus (Baker). Journal of Experimental Marine Biology and Ecology, 42, 99-111.
Diaz, E.R., Kraufvelin, P. & Erlandsson, J., 2012. Combining gut fluorescence technique and spatial analysis to determine Littorina littorea grazing dynamics in nutrient-enriched and nutrient-unenriched littoral mesocosms. Marine Biology, 159 (4), 837-852.
Dodds, W.K. & Gudder, D.A., 1992. The ecology of Cladophora. Journal of Phycology, 28, 415-427.
Ekaratne, S.U.K. & Crisp, D.J., 1984. Seasonal growth studies of intertidal gastropods from shell micro-growth band measurements, including a comparison with alternative methods. Journal of the Marine Biological Association of the United Kingdom, 64, 183-210.
Evans, R.G., 1948. The lethal temperatures of some common British littoral molluscs. The Journal of Animal Ecology, 17, 165-173.
Fortes, M.D. & Lüning, K., 1980. Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod. Helgolander Meeresuntersuchungen, 34, 15-29.
Fraser, J.H., 1936. The occurrence, ecology and life-history of Tigriopus fulvus (Fischer). Journal of the Marine Biological Association of the United Kingdom, 20, 523-536.
Fretter, V. & Graham, A., 1994. British prosobranch molluscs: their functional anatomy and ecology, revised and updated edition. London: The Ray Society.
Gerson, U & Seaward, M.R.D., 1977. Lichen - invertebrate associations. In Lichen ecology (ed. M.R.D. Seaward), pp. 69-119. London: Academic Press.
Goss-Custard, S., Jones, J., Kitching, J.A. & Norton, T.A., 1979. Tide pools of Carrigathorna and Barloge Creek. Philosophical Transactions of the Royal Society. Series B: Biological Sciences, 287, 1-44.
Grenon, J.F. & Walker, G., 1981. The tenacity of the limpet, Patella vulgata L.: an experimental approach. Journal of Experimental Marine Biology and Ecology, 54, 277-308.
Hawkins, S. J. & Jones, H. D., 1992. Rocky Shores. London: Immel.
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.
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.
Hoare, R. & Hiscock, K., 1974. An ecological survey of the rocky coast adjacent to the effluent of a bromine extraction plant. Estuarine and Coastal Marine Science, 2 (4), 329-348.
Hruby, T. & Norton, T.A., 1979. Algal colonization on rocky shores in the Firth of Clyde. Journal of Ecology, 67, 65-77.
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.
Hyslop B.T. & Davies, M.S., 1998. Evidence for abrasion and enhanced growth of Ulva lactuca L. in the presence of colliery waste particles. Environmental Pollution, 101 (1), 117-121.
Hyslop, B.T., Davies, M.S., Arthur, W., Gazey, N.J. & Holroyd, S., 1997. Effects of colliery waste on littoral communities in north-east England. Environmental Pollution, 96 (3), 383-400.
JNCC (Joint Nature Conservation Committee), 1999. Marine Environment Resource Mapping And Information Database (MERMAID): Marine Nature Conservation Review Survey Database. [on-line] http://www.jncc.gov.uk/mermaid
Jones, W.E. & Babb, M.S., 1968. The motile period of swarmers of Enteromorpha intestinalis (L.) Link. British Phycological Bulletin, 3, 525-528.
Joosse, E.N.G., 1976. Littoral apterygotes (Collembola and Thysanura). In Marine insects (ed. L. Cheng), pp. 151-186. Amsterdam: North-Holland Publishing Company.
Kain, J.M., & Norton, T.A., 1990. Marine Ecology. In Biology of the Red Algae, (ed. K.M. Cole & Sheath, R.G.). Cambridge: Cambridge University Press.
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.
Kennison, R.L. & Fong, P., 2013. High amplitude tides that result in floating mats decouple algal distribution from patterns of recruitment and nutrient sources. Marine Ecology Progress Series, 494, 73-86.
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.
Kraufvelin, P., 2007. Responses to nutrient enrichment, wave action and disturbance in rocky shore communities. Aquatic Botany, 87 (4), 262-274.
Kylin, H., 1917. Kalteresistenze der Meerealen. Bericht der Deutschen Botanischen Gesellschafter, 35, 370-384.
Lazzaretto, I., Franco, F. & Battaglia, B., 1994. Reproductive behaviour in the harpacticoid copepod Tigriopus fulvus. Hydrobiologia, 292-293, 229-234.
Le Quesne W.J.F. 2005. The response of a protandrous species to exploitation, and the implications for management: a case study with patellid limpets. PhD thesis. University of Southampton, Southampton, United Kingdom.
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.
Lewis, J.R., 1964. The Ecology of Rocky Shores. London: English Universities Press.
Lewis, S., Handy, R.D., Cordi, B., Billinghurst, Z. & Depledge, M.H., 1999. Stress proteins (HSPs): methods of detection and their use as an environmental biomonitor. Ecotoxicology, 8, 351-368.
Lewis, S., May, S., Donkin, M.E. & Depledge, M.H., 1998. The influence of copper and heat shock on the physiology and cellular stress response of Enteromorpha intestinalis. Marine Environmental Research, 46, 421-424.
Little, C. & Kitching, J.A., 1996. The Biology of Rocky Shores. Oxford: Oxford University Press.
Little, C., Partridge, J.C. & Teagle, L., 1991. Foraging activity of limpets in normal and abnormal tidal regimes. Journal of the Marine Biological Association of the United Kingdom, 71, 537-554.
Littler, M.M., Martz, D.R. & Littler, D.S., 1983. Effects of recurrent sand deposition on rocky intertidal organisms: importance of substrate heterogeneity in a fluctuating environment. Marine Ecology Progress Series. 11 (2), 129-139.
Lobban, C.S. & Harrison, P.J., 1997. Seaweed ecology and physiology. Cambridge: Cambridge University Press.
Lüning, K., 1990. Seaweeds: their environment, biogeography, and ecophysiology: John Wiley & Sons.
Lüning, K., 1984. Temperature tolerance and biogeography of seaweeds: the marine algal flora of Helgoland (North Sea) as an example. Helgolander Meeresuntersuchungen, 38, 305-317.
Marchan, S., Davies, M.S., Fleming, S. & Jones, H.D., 1999. Effects of copper and zinc on the heart rate of the limpet Patella vulgata (L.) Comparative Biochemistry and Physiology, 123A, 89-93.
Marshall, D.J. & McQuaid, C.D., 1989. The influence of respiratory responses on the tolerance to sand inundation of the limpets Patella granularis L.(Prosobranchia) and Siphonaria capensis Q. et G.(Pulmonata). Journal of Experimental Marine Biology and Ecology, 128 (3), 191-201.
Marshall, D.J. & McQuaid, C.D., 1993. Effects of hypoxia and hyposalinity on the heart beat of the intertidal limpets Patella granvlaris (Prosobranchia) and Siphonaria capensis (Pulmonata). Comparative Biochemistry and Physiology Part A: Physiology, 106 (1), 65-68
Martinez, B., Pato, L.S. & Rico, J.M., 2012. Nutrient uptake and growth responses of three intertidal macroalgae with perennial, opportunistic and summer-annual strategies. Aquatic Botany, 96 (1), 14-22.
Martins, I., Oliveira, J.M., Flindt, M.R. & Marques, J.C., 1999. The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal). Acta Oecologica, 20 (4), 259-265.
McAllen, R., 1999. Enteromorpha intestinalis - a refuge for the supralittoral rockpool harpacticoid copepod Tigriopus brevicornis. Journal of the Marine Biological Association of the United Kingdom, 79, 1125-1126.
McAllen, R., Taylor, A.C. & Davenport, J., 1999. The effects of temperature and oxygen partial pressure on the rate of oxygen consumption of the high-shore rock pool copepod Tigriopus brevicornis. Comparative Biochemistry and Physiology A, 123, 195-202.
Morris, S. & Taylor, A.C. 1983. Diurnal and seasonal variations in physico-chemical conditions within intertidal rock pools. Estuarine, Coastal and Shelf Science, 17, 339-355.
Moss, B. & Marsland, A., 1976. Regeneration of Enteromorpha. British Phycological Journal, 11, 309-313.
Moss, B.L. & Woodhead, P., 1975. The effect of two commercial herbicides on the settlement, germination and growth of Enteromorpha. Marine Pollution Bulletin, 6, 189-192.
Naylor, E. & Slinn, D.J., 1958. Observations on the ecology of some brackish water organisms in pools at Scarlett Point, Isle of Man. Journal of Animal Ecology, 27, 15-25.
Niesenbaum R.A., 1988. The ecology of sporulation by the macroalga Ulva lactuca L. (chlorophyceae). Aquatic Botany, 32, 155-166.
Pedersen, M.F., Borum, J. & Fotel, L. F., 2009. Phosphorus dynamics and limitation of fast and slow-growing temperate seaweeds in Oslofjord, Norway. Marine Ecology Progress Series, 399, 103-115
Picton, B.E. & Costello, M.J., 1998. BioMar biotope viewer: a guide to marine habitats, fauna and flora of Britain and Ireland. [CD-ROM] Environmental Sciences Unit, Trinity College, Dublin., http://www.itsligo.ie/biomar/
Pinn, E.H. & Rodgers, M., 2005. The influence of visitors on intertidal biodiversity. Journal of the Marine Biological Association of the United Kingdom, 85 (02), 263-268.
Povey, A. & Keough, M.J., 1991. Effects of trampling on plant and animal populations on rocky shores. Oikos, 61: 355-368.
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.
Raffaelli, D. & Hawkins, S., 1999. Intertidal Ecology 2nd edn.. London: Kluwer Academic Publishers.
Rai, L., Gaur, J.P. & Kumar, H.D., 1981. Phycology and heavy-metal pollution. Biological Reviews, 56, 99-151.
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.
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.
Ribeiro, P.A., Xavier, R., Santos, A.M. & Hawkins, S.J., 2009. Reproductive cycles of four species of Patella (Mollusca: Gastropoda) on the northern and central Portuguese coast. Journal of the Marine Biological Association of the United Kingdom, 89 (06), 1215-1221.
Rice, H., Leighty, D.A. & McLeod, G.C., 1973. The effects of some trace metals on marine phytoplankton. CRC Critical Review in Microbiology, 3, 27-49.
Robles, C., 1982. Disturbance and predation in an assemblage of herbivorous Diptera and algae on rocky shores. Oecologia, 54 (1), 23-31.
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.
Sfriso, A., Marcomini, A. & Pavoni, B., 1987. Relationships between macroalgal biomass and nutrient concentrations in a hypertrophic area of the Venice Lagoon. Marine Environmental Research, 22 (4), 297-312.
Shanks, A.L. & Wright, W.G., 1986. Adding teeth to wave action- the destructive effects of wave-bourne rocks on intertidal organisms. Oecologia, 69 (3), 420-428.
Smith, G.M., 1947. On the reproduction of some Pacific coast species of Ulva. American Journal of Botany, 34, 80-87.
Smith, J.E. (ed.), 1968. 'Torrey Canyon'. Pollution and marine life. Cambridge: Cambridge University Press.
Southward, A.J. & Southward, E.C., 1978. Recolonisation of rocky shores in Cornwall after use of toxic dispersants to clean up the Torrey Canyon spill. Journal of the Fisheries Research Board of Canada, 35, 682-706.
Southward, A.J., Hawkins, S.J. & Burrows, M.T., 1995. Seventy years observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. Journal of Thermal Biology, 20, 127-155.
Storey, K.B., Lant, B., Anozie, O.O. & Storey, J.M., 2013. Metabolic mechanisms for anoxia tolerance and freezing survival in the intertidal gastropod, Littorina littorea. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 165 (4), 448-459.
Sverdrup, H.U., Johnson, M.W. & Fleming, R.H., 1942. The Oceans. New York: Prentice Hall.
Tolhurst, L.E., Barry, J., Dyer, R.A. & Thomas, K.V., 2007. The effect of resuspending sediment contaminated with antifouling paint particles containing Irgarol 1051 on the marine macrophyte Ulva intestinalis. Chemosphere, 68 (8), 1519-1524.
UKTAG, 2014. UK Technical Advisory Group on the Water Framework Directive [online]. Available from: http://www.wfduk.org
Vadas, R.L., Johnson, S. & Norton, T.A., 1992. Recruitment and mortality of early post-settlement stages of benthic algae. British Phycological Journal, 27, 331-351.
Vadas, R.L., Keser, M. & Rusanowski, P.C., 1976. Influence of thermal loading on the ecology of intertidal algae. In Thermal Ecology II, (eds. G.W. Esch & R.W. McFarlane), ERDA Symposium Series (Conf-750425, NTIS), Augusta, GA, pp. 202-212.
Van den Hoek, C., 1982. The distribution of benthic marine algae in relation to the temperature regulation of their life histories. Biological Journal of the Linnean Society, 18, 81-144.
Vaudrey, J.M.P., Kremer, J.N., Branco, B.F. & Short, F.T., 2010. Eelgrass recovery after nutrient enrichment reversal. Aquatic Botany, 93 (4), 237-243.
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.
Wells, E., Best, M., Scanlan, C. & Foden, J., 2014. Opportunistic Macroalgae Blooming. Water Framework Directive- development of classification tools for ecological assessment., Water Framework Directive-United Kingdom Technical Advisory Group (WFD-UKTAG),
This review can be cited as:
Last Updated: 31/03/2016