Brissopsis lyrifera and Amphiura chiajei in circalittoral mud

27-10-2004
Researched byGeorgina Budd Refereed byDr Karin Hollertz
EUNIS CodeA5.363 EUNIS NameBrissopsis lyrifera and Amphiura chiajei in circalittoral mud

Summary

UK and Ireland classification

EUNIS 2008A5.363Brissopsis lyrifera and Amphiura chiajei in circalittoral mud
EUNIS 2006A5.363Brissopsis lyrifera and Amphiura chiajei in circalittoral mud
JNCC 2004SS.SMu.CFiMu.BlyrAchiBrissopsis lyrifera and Amphiura chiajei in circalittoral mud
1997 BiotopeSS.CMU._.BriAchiBrissopsis lyrifera and Amphiura chiajei in circalittoral mud

Description

Mud in deep offshore, or shallower stable near shore, waters can be characterized by the urchin Brissopsis lyrifera and the brittle star Amphiura chiajei. This community is very similar to CMS.AbrNucCor and CMS.AfilEcor but tends to occur in deeper and siltier muds. Transitional communities between the two may contain large numbers of Turritella. In certain areas of the UK such as the northern Irish Sea, this community may also contain Nephrops norvegicus and can consequently be the focus for fishing activity (Mackie et al., 1995). Where intense benthic dredge fishing activity occurs populations of the indicator species, Brissopsis lyrifera may be depressed, although broken tests may still remain (E.I.S. Rees pers. comm., 1997; M. Costello pers. comm., 1997). This community is the 'Boreal Offshore Mud Association' and 'Brissopsis - Chiajei' communities described by other workers (Petersen, 1918; Jones, 1950). (Information taken from the Marine Biotope Classification for Britain and Ireland, Version 97.06: Connor et al., 1997a, b).

Recorded distribution in Britain and Ireland

CMU.BriAchi has a widespread but scattered distribution occurring in the presence of fine silts and clays. 'Brissopsis lyrifera - Amphiura chiajei' associations are recorded in the North Sea, off the Northumbrian coast, at the edge of the Celtic Deep, in the north-east and north-west regions of the Irish Sea and in some Scottish sea lochs.

Depth range

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Additional information

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Habitat review

Ecology

Ecological and functional relationships

  • The presence of the characterizing and other species in this biotope is primarily determined by the occurrence of a suitable substratum rather than by interspecific interactions. Brissopsis lyrifera and Amphiura chiajei are functionally dissimilar and are not necessarily associated with each other but for their occurrence in the same muddy sediments. Hollertz et al. (1998) found evidence of indirect competition between Brissopsis lyrifera and Amphiura chiajei. Decreased body and gonad growth rates in Amphiura chiajei were reported in the presence of Brissopsis lyrifera, possibly indicating that Brissopsis lyrifera may be a superior competitor for food, or that the deeper burrowing activity of Brissopsis lyrifera disturbs Amphiura chiajei
  • Bioturbation is particularly important in controlling chemical, physical and biological processes in marine sediments, especially when the influences of physical disturbances such as wave action or strong currents are minimized (Widdicombe & Austen, 1999). Hollertz (1998) estimated the turnover rate of sediment by Brissopsis lyrifera to be 8.0 cm² per hour, thus it is likely that Brissopsis lyrifera plays an important role in the enhancement of species heterogeneity in an otherwise largely homogenous environment.
    Brissopsis lyrifera is reported to increase meiobenthic species abundance and diversity and have a density dependent effect upon the community structure of meiobenthic nematode communities (Widdicombe & Austen, 1998; Austen & Widdicombe, 1998). The presence of Brissopsis lyrifera also significantly influenced nutrient fluxes of nitrogen and phosphorus at the sediment-water interface, owing to its burrowing activity promoting oxygenation of the substrata. Also with a high density of Brissopsis lyrifera (71 individuals per m²), silicate precipitation from the water column was observed to increase, probably owing to continuous bioturbation exposing a greater volume of sediment to the light, enabling autotrophs such as diatoms and radiolarians, to exist deeper in the substrata rather than as a thin surface film, increasing the biological demand for dissolved silicates (Widdicombe & Austen,1998)
  • The burrowing and feeding activities of Brissopsis lyrifera and Amphiura chiajei and other macrofauna, are likely to modify the fabric and increase the mean particle size of the upper layers of the substrata by aggregation of fine particles into faecal pellets. Such actions create a more open sediment fabric with a higher water content which affects the rigidity of the seabed (Rowden et al., 1998). Such alteration of the substratum surface can affect rates of particle resuspension.
  • Most of the species living in deep mud biotopes are generally cryptic so are protected to some extent from visual surface predators. However, the arm tips of Amphiura chiajei are an important food source for demersal fish and Nephrops norvegicus providing significant energy transfer to higher trophic levels. Munday (1993) examined the occurrence and significance of arm regeneration in Amphiura chiajei in a population from western Ireland. Biomass assays revealed that regenerative tissue accounted for up to 57.9% of total body weight with an overall mean of 4.21±0.3 arms per individual regenerating. Increased nutrients leading to increased primary production may contribute to an accumulation of hydrophobic contaminants in Amphiura chiajei and their transfer to higher trophic levels (Gunnarsson & Skold, 1999).
  • Nephrops norvegicus is eaten by a variety of bottom-feeding fish, including cod, haddock, skate and lesser spotted catshark (dog fish). There are also numerous records of fish predation on thalassinidean mud shrimps such as Calocaris macandreae which has been found in the stomachs of cod and haddock. Nephrops norvegicus is carnivorous, feeding on brittle stars, polychaetes and other crustaceans such as Calocaris macandreae.
  • The bodies of shrimps can offer a substratum for colonization. The ctenostome bryozoan Triticella flava grows a dense 'furry' covering on the antennae, mouthparts and legs of Calocaris macandreae (Hughes, 1998(b)), whilst the mouthparts of Nephrops norvegicus harbour a small commensal sessile animal, the newly described Symbion pandora (Conway Morris, 1995).

Seasonal and longer term change

  • Amphiura chiajei is a long lived species. Particular cohorts (resultant of a dense and successful larval settlement) may dominate an area for over 10 years and is unlikely to show any significant regular seasonal change in abundance or biomass. However, populations of Amphiura chiajei seem to be periodically affected by winter cold. Mean densities of Amphiura chiajei in Killary Harbour, west coast of Ireland, decreased following months with the lowest recorded bottom temperatures, 4°C and 6°C, for February 1986 and January 1987 respectively. Intolerance of the acute change and depressed temperatures on the part of some older individuals probably led to their demise (Munday & Keegan, 1992).
  • There are daily patterns of activity in some species. For example, in shallower water, Nephrops norvegicus usually remain within their burrows by day and emerge at dusk to forage during the night. The animals return to their burrows around sunrise. However, in deeper water (> 100 m) this activity rhythm is reversed, and the animals are more active by day.
  • The distribution of Nephrops norvegicus shows some seasonality. In Loch Sween, Nephrops burrows were aggregated in groups during the late summer, which then broke up into a random distribution during the winter (Tuck et al., 1994). Such aggregations may result when burrow complexes formed when juvenile animals settle in pre-existing adult systems, and later extend their own burrows into other areas.

Habitat structure and complexity

  • The biotope has very little surface structural complexity as most species are infaunal, however, the bioturbating megafauna can create considerable structural complexity below the surface, relative to sediments that lack such animals. A low-energy hydrodynamic regime is a prerequisite for the existence of the fine sedimentary substrata about which some fauna are highly selective. For instance, Amphiura chiajei occurs in greatest density in habitats with a silt/clay content of 80-90% in association with an organic carbon content of 5-7%, whilst Calocaris macandreae only occurs in areas where silt/clay content is greater than 20%, highest densities occur where silt/clay content greater than 60% (Buchanan, 1963).
  • Burrows and mounds created by burrowing megafauna may be a conspicuous feature of the sediment surface with arm tips of Amphiura chiajei stretching out over the surface but these are not likely to provide a significant habitat for other fauna. However, the bodies of shrimps can offer a substratum for colonization (see ecological relationships).
  • Most species living within the sediment are restricted to the area above the anoxic layer, the depth of which will vary depending upon sediment particle size and organic content. Some structural complexity is provided by the burrows of macrofauna. Brissopsis lyrifera maintains a respiratory funnel to the surface, whilst the burrows of Calocaris macandreae and Nephrops norvegicus are more complex. Calocaris macandreae constructs a system of U-shaped tunnels which may reach a depth of 21 cm. Burrows of Nephrops norvegicus may be very large, with tunnels over a metre in length and up to 10 cm in diameter, whilst simple burrows consist of a straight or T-shaped tunnel descending at a shallow angle and penetrating the sediment to a depth of between 20-30 cm. Burrows and the bioturbatory activity that creates them allows a much larger volume of sediment to become oxygenated, enhancing the survival and diversity of a considerable variety of smaller infaunal species (Pearson & Rosenberg, 1978).
  • Deposit feeders, sort and process sediment particles and may result in destabilization of the sediment, which inhibits survival of suspension feeders. This can result in a change in the vertical distribution of particles in the sediment that may facilitate vertical stratification of some species with particle size preferences. Vertical stratification of species according to sediment particle size has been observed in some soft-sediment habitats (Petersen, 1977).

Productivity

Macroalgae are absent from CMU.BriAchi and consequently productivity is mostly secondary derived from detritus and organic material, although shallower sites may develop an extensive growth of benthic diatoms in the summer (David Hughes, pers. comm.).
Allochthonous organic material is derived from anthropogenic activity (e.g. sewerage) and natural sources (e.g. plankton, detritus). Autochthonous organic material is formed by benthic microalgae (microphytobenthos e.g. diatoms and euglenoids) and heterotrophic micro-organism production. Organic material is degraded by micro-organisms and the nutrients recycled. The high surface area of fine particles provides surface for the microflora.
Buchanan & Warwick (1974) obtained an estimate of the benthic macrofaunal production in the offshore mud off the Northumberland coast between 1971 - 1972. Eighteen species accounted for 90% of all animals, twelve being polychaetes. Although Calocaris macandreae was the single biomass dominant, polychaetes were responsible for the bulk of the biomass overall. The biomass averaged 3.98 g m², and was slightly lower in winter (3.4 - 3.8 g m²) than summer (4.2 - 4.5 g m²). Larger species with individual weights over 100 mg only occurred sporadically in small numbers, and accounted for 22% of the total biomass. In order of production they were: Ammotrypane aulogaster, Heteromastus filiformis, Spiophanes kroyeri, Glycera rouxi, Calocaris macandreae, Abra nitida, Lumbrineris fragilis and Chaetozone setosa. Their combined annual production was estimated to be 1432 mg m².
Of the species characteristic of the CMU.BriAchi biotope, Brissopsis lyrifera and Calocaris macandreae were the only significant producers, 108 mg m² /yr. and 142 mg m² /yr. respectively. The population of Amphiura chiajei in this study had been in decline, between 1961 and 1963 Amphiura chiajei density was 12-15 individuals per m², in 1971 only 2 individuals per m² were recorded. Owing to the species low productivity in this instance the authors discounted Amphiura chiajei from their estimates. However, the arms of Amphiura chiajei are an important food source for demersal fish and Nephrops norvegicus providing significant energy transfer to higher trophic levels. Densities of ca 700 Amphiura chiajei per m² were reported by Keegan & Mercer (1986) in Killary Harbour, Ireland, so the species is likely to be a significant producer in other instances. The estimated total production for the macrofauna was 1738 mg m² per annum.

Recruitment processes

  • In Brissopsis lyrifera the sexes are separate and fertilization external, with the development of a pelagic larva (Fish & Fish, 1996). The fact that Brissopsis lyrifera is the only heart urchin likely to be found in muddy sediments indicates that the larvae are highly selective, and as Brissopsis lyrifera is a burrower the larval phase is the main dispersive mechanism of the urchin. Echinoderm larvae generally undergo a complicated and protracted metamorphosis. For instance, the larvae of other echinoderms, Echinocardium cordatum and Echinus esculentus remain in the plankton for 40 and 46-60 days respectively (Kashenko, 1994; MacBride, 1914). Thus the larvae of Brissopsis lyrifera probably remain in the plankton for a sufficient length of time to disperse from the location of spawning, or to repopulate an area (Nichols, 1969). However, it is likely that the low-energy hydrodynamic regime of the biotope serves to maintain the benthic population, as larvae are retained and settle back into the parent population. From his observations made off the Northumbrian coast, Buchanan (1967) describes Brissopsis lyrifera as a highly productive, fast growing but short lived species. It becomes sexually mature at around 4 years (test length > 60 mm), spawns in late summer / autumn and dies shortly afterwards. Specimens have not been observed to survive and breed for a second time.
  • Amphiura chiajei reaches sexual maturity after four years and there is a seasonal cycle in gonad development. Spawning occurs between late summer and middle autumn (Fenaux, 1970). In the laboratory, Fenaux (1970) observed a complete larval metamorphosis to take only 8 days at 18°C. It is not clear whether this is representative of field conditions, at cooler temperatures metamorphosis may take longer, but such an apparently short planktonic existence would limit the species powers of dispersal. Despite spawning annually, successful recruitment tends to be sporadic. A heavy and successful settlement of Amphiura chiajei can dominate an area for over 10 years. The population of Amphiura chiajeithat Buchanan (1964) sampled off the Northumbrian coast showed no evidence of recruitment between 1958 and 1964, despite spawning annually. In such long-lived, adult dominated populations in apparently stable areas, Künitzer (1989) suggested that the survival of recruits was low owing to competition with established adults, which as non-selective surface deposit feeders may take their own newly settled juveniles (0.33 mm disc diameter) as a food item. Where established adult populations have become diminished, successful recruitment has been recorded (Munday & Keegan, 1992).
  • Female Nephrops norvegicus attain sexual maturity at 2.5-3 years of age at a carapace length of 22 mm (Howard, 1989; Bailey et al., 1986). Males become mature after 3 years at a carapace length of 25 mm. In Scottish waters the eggs are spawned and fertilized between August and November and carried by the females until the larvae hatch between April and August. The larvae spend about 50 days in the plankton before settlement. The juveniles appear to preferentially take up residence in existing adult burrows, constructing their burrows as an extension of these (Tuck et al., 1994).
  • Calocaris macandreae is a protandrous hermaphrodite (initially male, becoming female in later life) producing eggs between January and February that hatch between September and October. Approximately 100 eggs are produced in each batch and the large larvae have no free-swimming phase before settlement. Individual Calocaris macandreae are very long-lived (9-10 years) and slow growing. It does not mature until five years of age, and only produces two or three batches of eggs in a lifetime. Owing to this life history pattern populations tend to be very stable in number over a 10 year period (Buchanan, 1963; 1974).

Time for community to reach maturity

Limited evidence concerning the community development of this biotope was found. The burrowing megafauna that characterize the biotope vary in their reproductive strategies and longevity. Brissopsis lyrifera is short lived (4 years) but fecund and shows clear evidence of successful and consecutive annual recruitment (Buchanan, 1967). Individuals become sexually mature in their forth year. Amphiura chiajei is longer lived than Brissopsis lyrifera and reaches sexual maturity in its forth year, thus the population structure of these species will not reach maturity for at least this length of time. Once established a cohort of Amphiura chiajei can dominate a population, even inhibiting its own consecutive recruitment, for up to 10 years. Time to reach sexual maturity is longer in Nephrops norvegicus, about 2.5 - 3 years and for the very long-lived Calocaris macandreae individuals off the coast of Northumberland did not become sexually mature until five years of age, and produced only two or three batches of eggs in their lifetime (Buchanan, 1963; 1974). In the biotope, polychaetes account for the vast proportion of the biomass, and these are likely to reproduce annually, be shorter lived and reach maturity much more rapidly. Most of the characterizing species reproduce regularly but recruitment is often sporadic owing to interference competition with established adults of the same and other species.

Owing to the fact that the characterizing species take between 3 and 5 years to reach sexual maturity, it is likely that the time for the overall community to reach a fully diverse state will also be several years. It is likely that the low-energy hydrodynamic regime is an important factor in the maintenance of stable benthic populations in this biotope, as larvae are retained in the vicinity of the parent population.

Additional information

None

Preferences & Distribution

Recorded distribution in Britain and IrelandCMU.BriAchi has a widespread but scattered distribution occurring in the presence of fine silts and clays. 'Brissopsis lyrifera - Amphiura chiajei' associations are recorded in the North Sea, off the Northumbrian coast, at the edge of the Celtic Deep, in the north-east and north-west regions of the Irish Sea and in some Scottish sea lochs.

Habitat preferences

Depth Range
Water clarity preferences
Limiting Nutrients No information found
Salinity
Physiographic
Biological Zone
Substratum
Tidal
Wave
Other preferences High silt/clay sediment fraction.

Additional Information

There is some doubt over records from the south coast. Holme (1961, 1966) inferred localized, usually inshore, occurrence of this community but with very few locations identified.

Species composition

Species found especially in this biotope

    Rare or scarce species associated with this biotope

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    Additional information

    Sensitivity reviewHow is sensitivity assessed?

    Explanation

    Brissopsis lyrifera and Amphiura chiajei are both important characterizing species in this biotope. However, owing to its bioturbatory activity which enhances local meiofaunal heterogeneity Brissopsis lyrifera is given key functional status. The burrowing mud shrimp, Calocaris macandreae, and Norway lobster, Nephrops norvegicus, are also important species within the biotope because their deeper burrows enhance the oxygenation of the substratum and enhance the survival of a variety of small species (Pearson & Rosenberg, 1978). In the absence of sensitivity information for Calocaris macandreae, Callianassa subterranea will be used as a surrogate species where appropriate.

    Species indicative of sensitivity

    Community ImportanceSpecies nameCommon Name
    Important characterizingAmphiura chiajeiBrittle star
    Key functionalBrissopsis lyriferaHeart urchin
    Important otherCalocaris macandreaeMud shrimp
    Important otherNephrops norvegicusNorway lobster

    Physical Pressures

     IntoleranceRecoverabilitySensitivitySpecies RichnessEvidence/Confidence
    High Moderate Moderate Major decline High
    Species within the CMU.BriAchi biotope are infaunal and will be lost if the substratum is removed so the overall intolerance of the biotope has been recorded as high. Although some species are mobile e.g. Calocaris macandreae and Nephrops norvegicus, if disturbed they are likely to seek refuge within a burrow within the substratum and so are also likely to be removed. The characterizing species do not reach sexual maturity for several years and recovery has been assessed to be moderate (see additional information below).
    Low Immediate Not sensitive No change Moderate
    The biotope will probably have a low intolerance to smothering by 5 cm of sediment because the characterizing species are all infaunal burrowers. There may be some energetic cost expended to either re-establish burrow openings in the case of Calocaris macandreae and Nephrops norvegicus, or to self-clean feeding apparatus though this is not likely to be significant. The biotope is likely to be more intolerant of smothering by viscous or impenetrable materials e.g. smothering by sediment of a coarser texture may affect burrowing and feeding. At the benchmark level, recovery of the community from smothering is assessed to be immediate.
    Tolerant* Not relevant Not sensitive* Rise Moderate
    Suspension feeders are not found within the biotope so clogging of feeding apparatus by suspended sediment is not a consideration. Brissopsis lyrifera, Amphiura chiajei, Calocaris macandreae and Turritella communis are burrowing infauna and non-selective surface and sub-surface deposit feeders. For most benthic deposit feeders, food is suggested to be a limiting factor for body and gonad growth, at least between events of sedimentation of fresh organic matter (Hargrave, 1980; Tenore, 1988). Consequently, an increase in the suspended matter settling out from the water column to the substratum may increase food availability. This suggests that an increase in siltation may be beneficial and the biotope is not considered to be sensitive.
    Low Moderate Not relevant Decline Moderate
    A decrease in the suspended sediment and hence siltation will reduce the flux of particulate material to the seabed. Since this includes organic matter the supply of food to the biotope would probably also be reduced. However, the benchmark states that this change would only occur for one month and therefore a decrease in siltation would be unlikely to cause a significant alteration to species composition. Therefore intolerance has been assessed to be low.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    The biotope only occurs in the circalittoral zone (below 10m) and is not subject to desiccation.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    The biotope only occurs in the circalittoral zone (below 10m) and is not likely to be subjected to a change in emergence regime.
    Not sensitive* Not relevant
    The biotope only occurs in the circalittoral zone (below 10m) and is not likely to be subjected to a change in emergence regime.
    Intermediate Moderate Moderate Minor decline Moderate
    The presence of the biotope is determined by a low energy hydrodynamic regime facilitating the deposition of cohesive fine silts and clays. Following an increase in water flow rate only the surface sediments are likely to be winnowed away in a unidirectional flow. The lower substratum inhabited by mature specimens of Brissopsis lyrifera and Amphiura chiajei is likely to remain unchanged. However, the settlement of the planktonic larvae of these key species may be inhibited owing to re-suspension along with particulate matter. Consequently the viability of the population may be reduced. Furthermore the deposit feeding community may experience a reduction in food availability owing to reduced deposition of organic matter. Intolerance to increased water flow rate has been assessed to be intermediate. On return to prior conditions, specimens of the characterizing species will have remained and are likely to repopulate via successful larval settlement. However, attainment of a fully diverse community is likely to take several years and recovery has been assessed to be moderate (see additional information below).
    Tolerant Not sensitive* No change Moderate
    The presence of the biotope is determined by a low energy hydrodynamic regime facilitating the deposition of fine silts and clays, hence the community is not likely to be directly intolerant of a decrease in water flow rate. Sediments may become muddier owing to increased settlement of particulate matter. However, as deposit feeders are the dominant trophic group such additional material may be utilizable as a food resource and the community may benefit indirectly.
    Intermediate High Low Minor decline Moderate
    In shallower locations e.g. sea lochs, sedimentary biotopes typically experience seasonal changes in temperature of about 10°C (5-15°C) (Hughes, 1998b) and it is likely that the CMU.BriAchi community would be tolerant of a long term chronic temperature increase. For most offshore burrowing species, temperature changes in the water column are likely to buffered by the insulation offered by the substratum and the depth of overlying water. Furthermore, a temperature increase may enhance growth and fecundity. Muus (1981) showed that juvenile Amphiura filiformis are capable of much higher growth rates in experiments with temperatures between 12 and 17°C (unlimited food supply). Juvenile disc diameter increased from 0.5 to 3.0 mm in 28 weeks under these conditions compared to over 2 years in the North Sea. Mean summer temperatures of 14°C and an apparent abundant food supply may also account for the early rapid growth of Amphiura chiajei in Killary Harbour (Munday & Keegan, 1992). In Brissopsis lyrifera, processes such as mobility, sediment turnover and remineralization may increase (K. Hollertz, pers. comm., Hollertz & Duchêne, 2001). Hollertz & Duchê (2001) found that in Brissopsis lyrifera, the amount of reworked sediment due to burrowing almost doubled from 14 to 22 ml/l sediment per hour when the temperature increased from 7 to 13 °C. This temperature increase also saw the amount of ingested sediment increase from 0.02 to 0.08 g dry sediment per hour. However, increased water temperature may enhance microbial decomposition within the substratum and promote deoxygenation, to which Brissopsis lyrifera is intolerant. Owing to the fact that the biotope is subtidal, where wide and rapid variations in temperature, such as those experienced in the intertidal, are not common, the community is likely to be more intolerant of an acute temperature increase of 5°C and intolerance has been assessed to be intermediate. Recovery has been assessed to be high since members of the community are likely to remain to revitalize the population (see additional information below).
    Intermediate High Low Minor decline Low
    In shallower locations e.g. sea lochs, sedimentary biotopes typically experience seasonal changes in temperature of about 10°C (5-15°C) (Hughes, 1998b) and it is likely that the CMU.BriAchi community would be tolerant of a long term chronic temperature decrease. For most offshore burrowing species temperature changes in the water column are likely to buffered to some extent by the insulation offered by the substratum and the depth of overlying water. However, burrowing itself has been found to be significantly affected by temperature in Brissopsis lyrifera. Hollertz & Duchêne (2001) found that Brissopsis lyrifera reworked almost half the amount of sediment per hour at 7 °C compared to activity at 14 °C. Furthermore, Brissopsis lyrifera maintains a continuous contact with the overlying water column through the funnel (Hollertz, 2002). Also, the biotope community seems to be periodically affected by severe winters. During the winter of 1962-1963 a few dead Nephrops norvegicus were caught in the North Sea, although the majority were caught alive (Crisp, 1964). Mean densities of Amphiura chiajei in Killary Harbour, west coast of Ireland, decreased following months with the lowest recorded bottom temperatures, 4°C and 6°C, for February 1986 and January 1987 respectively. Intolerance of the acute change and depressed temperatures on the part of some of the older individuals probably led to their demise (Munday & Keegan, 1992). Low temperatures are also a limiting factor for breeding which occurs in the warmest months in the UK. Temperature tolerances of Brissopsis lyrifera are unknown but low water temperatures have caused mass mortalities of other similar echinoderms, such as Echinocardium cordatum. In the severe winter of 1962-63 masses of dead Echinocardium cordatum were observed in regions of the North Sea and English Channel, although it was reported that living specimens were obtained easily enough by digging (Crisp, 1964). Therefore, intolerance has been assessed to be intermediate as key species within the community appear to be periodically degraded by acute decreases in temperature. Recovery has been assessed to be high, as members of the community remain to revitalize the population.
    Low Very high Very Low No change Moderate
    The community is unlikely to be directly intolerant of the light attenuating effects of an increase in turbidity, however, for other related but indirect effects, see suspended sediment above. In the long term, increased turbidity may affect primary production by the microphytobenthos on the substratum surface depleting food availability. Furthermore, increased turbidity may hinder predation by visual predators such as Nephrops norvegicus, dab Limanda limanda, haddock Melanogrammus aeglefinus upon Amphiura chiajei, which provides an important link between the benthic and pelagic realms. There may be some increased energetic costs experienced by certain species, associated with increased turbidity, but effects are not likely to be significant and so intolerance has been assessed to be low. Recoverability is likely to be very high on return to conditions prior to the impact.
    Tolerant* Not sensitive No change Moderate
    The community is unlikely to be directly intolerant of increased light penetration of the water column caused by a decrease in turbidity. Greater light penetration of the water column may improve primary production by phytoplankton in the water column and contribute to secondary productivity via the production of detritus from which the community may benefit. For other related but indirect effects see decrease in suspended sediment above.
    High Very low / none Very High Major decline Moderate
    The CMU.BriAchi biotope occurs offshore and in sheltered near shore habitats where wave exposure is negligible, so the biotope is probably very intolerant of increased wave exposure. However, the factor is only likely to affect the biotope where it occurs at depths of less than 60 m, as the effects of wave action are attenuated with depth. Wave action resulting from storms may disturb the surface sediment. McIntosh (1875) reported specimens of Amphiura chiajei thrown on to West Sands, St. Andrews Bay after storms. Over the duration of a year increased wave exposure is likely to cause the substratum character to drastically alter, as wave action would penetrate the substratum to a greater depth, and become outside the habitat preference of the species. The community would no longer occur at that location. Intolerance has therefore been assessed to be high. Once fine sediments have been removed it would take a very long time for a suitable substratum to reform so recovery has been assessed to be very low.
    Tolerant Not sensitive* No change Moderate
    The CMU.BriAchi biotope occurs offshore and in sheltered near shore habitats where wave exposure is already negligible, so a reduction in wave exposure is not likely to have a direct impact upon the biotope community and intolerance has been assessed to be low.
    Tolerant Not relevant Not relevant No change Low
    No information concerning noise reception in the characterizing species of this biotope was found, but it is likely that the community will be not sensitive to noise disturbance at the benchmark level.
    Tolerant Not relevant Not relevant No change Very low
    Although some species within the community have visual perception e.g. Calocaris macandreae and Nephrops norvegicus, detecting the presence of boats or machinery, is likely to be beyond their visual acuity and the biotope community is assessed as not sensitive.
    Intermediate High Low Decline High
    The CMU.BriAchi biotope can be affected by fishing activity in areas such as the northern Irish Sea, where the community may also contain Nephrops norvegicus (Mackie et al., 1995). In areas of the North Sea where heavy demersal fishing for Nephrops norvegicus occurs, populations of Brissopsis lyrifera are likely to be reduced owing to damage inflicted to the 'test' by the fishing gear. Broken tests may be seen on the seabed (E.I.S. Rees, M. Costello, pers comm. to Connor et al., 1997). Similar evidence has been reported for other heart urchins. For example, Houghton et al. (1971), Graham (1955), de Groot & Apeldoorn (1971) and Rauck (1988) refer to significant trawl-induced mortality of heart urchin Echinocardium cordatum. A substantial reduction in the numbers of the species due to physical damage from scallop dredging has been observed (Eleftheriou & Robertson, 1992). Bergman & van Santbrink (2000) suggested that Echinocardium cordatum was one of the most vulnerable species to trawling. Bradshaw et al. (2000) suggested that fragile species such a urchins (e.g. Spatangus purpureus and Echinus esculentus), suffered badly from impact with a passing scallop dredge. Overall, species with brittle, hard tests are regarded to be sensitive to impact with scallop dredges (Kaiser & Spencer, 1995; Bradshaw et al., 2000).

    Brittlestars have fragile arms that are likely to be damaged by abrasion or physical disturbance. Amphiura chiajei burrows in the sediment and extends its arms across the sediment surface to feed. Ramsay et al., (1998) suggests that Amphiura species may be less susceptible to beam trawl damage than other species of echinoid or tube dwelling amphipods and polychaetes. Bergman & Hup (1992) for example, found that beam trawling in the North Sea had no significant direct effect on small brittlestars. Bradshaw et al. (2002) noted that the brittlestars Ophiocomina nigra, Ophiura albida and Amphiura filiformis had increased in abundance in a long-term study of the effects of scallop dredging in the Irish Sea. Brittlestars can tolerate considerable damage to arms and even the disc without suffering mortality and are capable of disc and arm regeneration so their recovery is likely to be rapid.

    Deeper burrowing crustaceans such as Calocaris macandreae may occasionally be displaced from burrow openings by towed gear (Atkinson, 1989). During long term monitoring of fishing disturbance on the Northumberland coast Frid et al. (1999) observed a decrease in the numbers of sedentary polychaetes, echinoid echinoderms and large (> 5 cm) brittlestars.

    Therefore, while brittlestars may increase in abundance in the long term, the dominant heart urchin species is likely to be reduced in abundance and an intolerance of intermediate has been recorded. Recovery is likely to be high, as members of the community are likely to remain and be able to repopulate. Brissopsis lyrifera may not regenerate as well as the brittle star (K. Hollertz, pers. comm.).

    Low Immediate Not sensitive No change Low
    Although not highly active Brissopsis lyriferaand Amphiura chiajei are burrowing infaunal species, as are Calocaris macandreae and Nephrops norvegicus. Following displacement to suitable sediments these species are likely to commence burrowing immediately provided that individuals are not damaged during displacement. The species will be exposed to predators for a short time so intolerance is assessed to be low.

    Chemical Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    High Moderate Moderate Decline High
    Effects caused by synthetic chemicals have been reported for some of the individual species in the CMU.BriAchi biotope. Dahllöf et al. (1999) studied the long term effects of tri-n-butyl-tin (TBT) on the function of a marine sediment system. TBT spiked sediment was added to a sediment that already had a TBT background level of approximately 27 ng/g (83 pmol TBT per g) and contained the following fauna: Amphiura spp., Brissopsis lyrifera and several species of polychaete. Within two days of treatment with a TBT concentration above 13.7 µmol / m² all species except the polychaetes had crept up to the surface and after six weeks these fauna had started to decay. Thus contamination from TBT is likely to result in the death of some intolerant species such as brittle stars and heart urchins. Amphiura chiajei is also known to bioaccumulate PCBs, although direct effects of synthetic chemicals on this species are unknown. (Gunnarsson & Skold, 1999). However, Walsh et al., (1986) observed inhibition of arm regeneration in another brittlestar, Ophioderma brevispina, following exposure to TBT at levels between 10 ng/l and 100 ng/l. Loizeau & Menesguen (1993), found that 8-15% of the PCB burden in dab, Limanda limanda, from the Bay of Seine could be explained by ophiuroid consumption. Thus Amphiura communities may play an important role in the accumulation, remobilization and transfer of PCBs and other sediment associated contamination to higher trophic levels. The key species seem to be highly intolerant of some chemical pollutants and may be lost from the biotope. In their absence the biotope would not be recognized so intolerance has been assessed to be high. In the absence of synthetic chemical contaminants re-population of the biotope is likely to occur, but owing for the time for the community to reach maturity recovery is assessed to be moderate.
    Heavy metal contamination
    Intermediate Moderate Moderate Decline Moderate
    Information concerning the effects of heavy metals on echinoderms is limited and no information specific to Brissopsis lyrifera and Amphiura chiajei was found. In Norwegian fjords Rygg (1985) found a relationship between species diversity in benthic fauna communities and sediment concentrations of heavy metals Cu, Pb and Zn. Cu in particular showed a strong negative correlation and the author suggested a cause-effect relationship. Those species not present at sites where Cu concentrations were greater than ten times the background level, such as Calocaris macandreae, Amphiura filiformis and the bivalve Nucula sulcata (also found in CMU.BriAchi), were assessed as non-tolerant species. Tolerant species were all polychaete worms. Polychaete worms are the dominant component of the biomass in the CMU.BriAchi biotope and thus may not be as sensitive as the characterizing species. Crompton (1997) reports that the concentrations above which mortality of crustaceans can occur is 0.01-0.1 mg/l for mercury, copper and cadmium, 0.1-1.0 mg/l for zinc, arsenic and nickel and 10 mg/l for lead and chromium. The biotope is considered to have an intermediate intolerance owing to the fact that heavy metal contamination of the sediments may change the faunal composition of the community and decrease overall species diversity. Some burrowing crustaceans, brittlestars and bivalves may disappear from the biotope and lead to an increasing dominance of polychaetes. In the absence of heavy metal contaminants re-population of the biotope is likely to occur, but owing for the time for the community to reach maturity recovery is assessed to be moderate.
    Hydrocarbon contamination
    High Moderate Moderate Decline High
    Amphiura chiajei was reported to be very intolerant of hydrocarbon contamination. Chronic sub-lethal effects were detected around the Beryl oil platform in the North Sea where the hydrocarbon content of the sediment was very low (<3 ppm total hydrocarbons in sediment), and Amphiura chiajei was excluded from areas nearer the platform with higher sediment hydrocarbon content (> 10 ppm) (Newton & McKenzie, 1998). As Amphiura chiajei is an important characterizing species within the biotope intolerance is assessed to be high, as in the absence of it the biotope would not be recognized. Brissopsis lyrifera is also likely to be intolerant of hydrocarbon pollution owing to exposure of the epidermis. Furthermore, Brissopsis lyrifera has a continuous water flow over the test so the exposure route through the epidermis may also be important (K. Hollertz, pers. comm., Hollertz, 2002). However, as a burrower and deposit feeder, ingestion of contaminated sediments is likely to be a more important route of exposure. A range of effects (mortalities, feeding/growth inhibition and embryological abnormalities) have been reported for other echinoderms following hydrocarbon exposure (reviewed by Suchanek, 1993). It is also likely that Crustacea such as Calocaris macandreae would be intolerant of hydrocarbons. The abundance of a similar species Callianassa subterranea was significantly reduced up to and over 1 km away from a site of oil drilling one year after drilling ceased (Daan et al., 1992). Therefore, intolerance has been assessed to be high. Re-population is likely following degradation of the contaminants but considered to be moderate (see additional information below).
    Radionuclide contamination
    No information Not relevant No information Not relevant Not relevant
    Investigations of bioturbation in radionuclide contaminated sediments on the Irish Sea floor near the Sellafield nuclear reprocessing plant found Nephrops norvegicus and Calocaris macandreae to be present (Hughes & Atkinson, 1997). There is insufficient information on the intolerance of Amphiura chiajei to radionuclides, although adult echinoderms, such as Ophiothrix fragilis, are known to be efficient concentrators of radionuclides (Hutchins et al., 1996). However, no information concerning the effects of such bioaccumulation was found.
    Changes in nutrient levels
    Tolerant* Not relevant Not sensitive* Rise Moderate
    Nutrient enrichment can enhance primary productivity in the water column and consequently generate organic detritus that falls to the sea bed. The characterizing species of the CMU.BriAchi biotope demonstrate a preference for substratum high in organic matter. Nilsson (1999) reported a positive response by Amphiura chiajei to increased organic enrichment (27 and 55 g/C/m², applied four times over eight weeks) demonstrable by an increase in arm tip regeneration rate. For benthic deposit feeders, food is suggested to be a limiting factor for body and gonad growth, at least between events of sedimentation of fresh organic matter (Hargrave, 1980; Tenore, 1988). Nilsson (1999) also found that Amphiura chiajei was able to utilize an increased input of organic matter for growth in conjunction with moderate hypoxia. Hollertz (1998) demonstrated increased surface deposit feeding activity for Brissopsis lyriferaafter the addition of organic matter and recorded an increase in growth. In Loch Sween, Scotland, where the organic content is about 5% and as high as 9% in some patches, the burrowing crustaceans Calocaris macandreae and Nephrops norvegicus are present in high densities (Atkinson, 1989). At the benchmark level, a 50% increase in nutrients as an annual average, the biotope community may benefit. In conditions of gross nutrient enrichment hypoxia becomes a factor of consideration, see oxygenation below.
    Not relevant Not relevant Not relevant Not relevant Very low
    The biotope CMU.BriAchi is found within fully marine subtidal locations and it is highly unlikely that the biotope would experience conditions of hypersalinity and in this instance the factor is considered not relevant. However, it is likely that key components of the biotope community would be intolerant of an increase in salinity. For instance, echinoderms such as Brissopsis lyrifera and Amphiura chiajei are stenohaline owing to the lack of an excretory organ and a poor ability to osmo- and ion-regulate causing body fluid to decrease when individuals are exposed to higher salinity (Stickle & Diehl, 1987).
    High Moderate Intermediate Decline Moderate
    The biotope CMU.BriAchi is found within fully marine subtidal locations. However, it is likely that key components of the biotope community would be intolerant of a decrease in salinity. For instance, echinoderms such as Brissopsis lyrifera and Amphiura chiajei are stenohaline owing to the lack of an excretory organ and a poor ability to osmo- and ion-regulate causing body fluid to increase when individuals are exposed to lower salinity (Stickle & Diehl, 1987). Pagett (1979), examined the tolerance of Amphiura chiajei to brackish water (0.5-30 psu) in specimens taken from Loch Etive, Scotland. Loch Etive is a sea loch subject to periods of reduced salinities owing to heavy rain and fresh-water runoff. Pagett (1979) found that specimens nearer freshwater influxes were more tolerant of reduced salinities than those nearer the open sea. Amphiura chiajei taken from an area of 24 psu had an LD50 of > 21 days for a 70% dilution (17 psu) and an LD50 of 8.5 days for a 50% dilution (12 psu). In comparison, specimens taken from an area with salinity 28.9 psu, had an LD50 of > 12.5 days for a 70% dilution (20 psu) and an LD50 of 6 days for a 50% dilution (14 psu). As Amphiura chiajei is mobile and burrows it may be able to avoid changes in salinity outside its preference, e.g. burrowing may help Amphiura chiajei to withstand depressed salinities owing to the 'buffering' effect of the substratum. However, as some mortalities were recorded for decreases in salinity over a time period less than the benchmark level, it is likely that Amphiura chiajei and the other characterizing species would be highly intolerant of a decrease of one category from the MNCR salinity scale for one year. The characterizing species do not reach sexual maturity for several years and recovery is likely to be moderate (see additional information below).
    High Moderate Moderate Decline High
    As infaunal burrowers the community lives in close association with hypoxic and even anoxic muddy substrata. In experiments, Amphiura chiajei exposed to decreasing oxygen levels only left its protected position in the sediment when oxygen levels fell below 0.54 mg l-1 (Rosenberg et al., 1991). This escape response increases its risk to predators. Mass mortality in a superficially similar species of ophiuroid, Amphiura filiformis from the south-east Kattegat was observed during severe hypoxic events (< 0.7 mg/l), while the abundance of Amphiura chiajei remained unchanged at the same site and time (Rosenberg & Loo, 1988). Nilsson (1999) maintained specimens of Amphiura chiajei in hypoxic conditions (1.8-2.2 mg/O2/l for eight weeks and recorded no deaths or witnessed specimens escaping to the surface. In moderately hypoxic conditions (1 mg/l) Nephrops norvegicuscompensates by increasing production of haemocyanin (Baden et al., 1990). In the laboratory this compensation lasted one week so at the level of the benchmark the species would not be killed. However, at levels of about 0.6 mg O2/l Nephrops died within four days. Catches of Nephrops norvegicus have been observed to be high in hypoxic conditions, probably because the animals are forced out of their burrows. Brissopsis lyrifera was reported as a species intolerant of hypoxia (Diaz & Rosenberg, 1995). It was recorded to leave its position within the substratum and lie exposed on the sediment surface in bottom waters with an oxygen concentration of 1 ml/O2/l (Baden et al., 1990). Thalassinidean mud-shrimps such as Calocaris macandreae are resistant to oxygen depletion. Anderson et al., (1991) reported oxygen availability within the burrow of Calocaris macandreae to be consistently severely low. It has a low oxygen consumption rate and responds to hypoxia by hyperventilation. However, at the benchmark level of 2 mg/O2/l for one week it is unlikely that the community composition would be greatly altered as many species are well adapted to conditions of hypoxia. However, as a key species, Brissopsis lyrifera, is especially intolerant of hypoxia and that the viability of some species may be affected if they are lying at the surface and exposed to predators or benthic trawls, intolerance has been recorded as high. On return to normoxia animals will rebury in to the substratum, but owing to the potential loss of the population of Brissopsis lyrifera, recoverability has been assessed to be moderate (see additional information below).

    Biological Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    Low Moderate Low Minor decline Moderate
    The only major biological agent known to affect a species in this biotope is the dinoflagellate parasite, Hematodinium sp., now prevalent in Nephrops norvegicus populations from the west of Scotland, Irish Sea and North Sea. The Hematodinium parasite occurs in the blood and connective tissue spaces and appears to cause death in the host by blocking the delivery of oxygen to the host's tissues (Taylor et al., 1996). Heavily-infested animals become moribund, spend more time out of their burrows and are probably less able to evade capture by predators or fishing gear. However, the ecological consequences of this infestation are unknown but evidence to date suggests that the Nephrops stocks have not been seriously affected (Hughes, 1999b). The occurrence of the ascothoracidan parasite Ulophysema öresundense (Brattström) has been observed in the body cavity of Brissopsis lyrifera (Brattström, 1946). This parasite may cause sexual castration but no further information concerning the effect of this parasite on the population was found.
    Not relevant Not relevant Not relevant Not relevant Moderate
    There are no records of any non-native species invading the biotope and it is considered not to be relevant.
    High Moderate Moderate Decline Moderate
    Neither Brissopsis lyrifera or Amphiura chiajei are targeted for collection or harvesting. However, Nephrops norvegicus, one of the species indicative of sensitivity, is the target of a large commercial fishery.

    Findings from the western Irish Sea suggest that the structure of some Nephrops populations may render them vulnerable to over-exploitation (Hughes, 1998(b). During the spring and summer a gyre (circulating water mass) forms, which coincides with the period when Nephrops larvae are present in the plankton. The gyre retained the larvae in the vicinity of the parent population, rather than being carried off by currents into areas of unsuitable substratum (Hill et al., 1997; Hill et al., 1996). The retention of larvae by the gyre may be essential for the maintenance of the local Nephrops population and it is possible that over-exploitation of Nephrops in this area could lead to a self-perpetuating population decline owing to a reduction in recruitment.

    In a study on the effects of otter trawling for Nephrops norvegicus on the benthos of locations in the Irish Sea and Scottish sea lochs, Ball et al., (2000) reported a reduction in the abundance of large-bodied and fragile organisms such as Brissopsis lyrifera and Amphiura chiajei and suggested that these species are particularly intolerant of trawling disturbance. An altered but stable community resulted, comprising of fewer species and reduced faunal diversity, consisting primarily of small polychaetes.
    In areas of the North Sea where heavy demersal fishing for Nephrops norvegicus occurs, populations of Brissopsis lyrifera are likely to be reduced owing to damage inflicted to the 'test' by the fishing gear. Broken tests may be seen on the seabed (E.I.S. Rees, M. Costello, pers comm. to Connor et al., 1997). Similar evidence has been reported for other heart urchins. For example, Houghton et al. (1971), Graham (1955), de Groot & Apeldoorn (1971) and Rauck (1988) refer to significant trawl-induced mortality of heart urchin Echinocardium cordatum. A substantial reduction in the numbers of the species due to physical damage from scallop dredging has been observed (Eleftheriou & Robertson, 1992). Bergman & van Santbrink (2000) suggested that Echinocardium cordatum was one of the most vulnerable species to trawling. Bradshaw et al. (2000) suggested that fragile species such a urchins (e.g. Spatangus purpureus and Echinus esculentus), suffered badly from impact with a passing scallop dredge. Overall, species with brittle, hard tests are regarded to be sensitive to impact with scallop dredges (Kaiser & Spencer, 1995; Bradshaw et al., 2000).
    Brittlestars have fragile arms that are likely to be damaged by abrasion or physical disturbance. Amphiura chiajei burrows in the sediment and extends its arms across the sediment surface to feed. Ramsay et al., (1998) suggests that Amphiura species may be less susceptible to beam trawl damage than other species of echinoid or tube dwelling amphipods and polychaetes. Bergman & Hup (1992) for example, found that beam trawling in the North Sea had no significant direct effect on small brittlestars. Bradshaw et al. (2002) noted that the brittlestars Ophiocomina nigra, Ophiura albida and Amphiura filiformis had increased in abundance in a long-term study of the effects of scallop dredging in the Irish Sea. Brittlestars can tolerate considerable damage to arms and even the disc without suffering mortality and are capable of disc and arm regeneration so their recovery is likely to be rapid. Deeper burrowing crustaceans such as Calocaris macandreae may occasionally be displaced from burrow openings by towed gear (Atkinson, 1989). During long term monitoring of fishing disturbance on the Northumberland coast Frid et al., (1999) observed a decrease in the numbers of sedentary polychaetes, echinoid echinoderms and large (> 5 cm) brittlestars.

    Therefore, while some authors have reported that brittlestars may increase in abundance in the long term, the dominant heart urchin species is likely to be reduced in abundance. Following the evidence of Ball et al. (2000), a high intolerance has been recorded. Recovery is likely to be moderate (see additional information), as members of the community are likely to remain and be able to repopulate. Brissopsis lyrifera may not regenerate as well as the brittle star (K. Hollertz, pers. comm.).

    High Moderate Moderate Decline High

    Additional information

    Recoverability:
    The biotope is likely to have a moderate capacity for recovery. The burrowing megafauna that characterize the biotope vary in their reproductive strategies and longevity. Brissopsis lyrifera is short lived (4 years) but is fecund and has shown clear evidence of successful and consecutive annual recruitment (Buchanan, 1967). Individuals become sexually mature in their forth year.

    Amphiura chiajei is longer lived than Brissopsis lyrifera and reaches sexual maturity in its forth year, thus the population structure of these species will not reach maturity for at least this length of time. Once established, a cohort of Amphiura chiajei can dominate a population, even inhibiting its own consecutive recruitment, for up to 10 years. Time to reach sexual maturity is longer in Nephrops norvegicus, about 2.5 - 3 years and for the very long-lived Calocaris macandreae individuals off the coast of Northumberland did not become sexually mature until five years of age, and produced only two or three batches of eggs in their lifetime. In the biotope, polychaetes account for the vast proportion of the biomass, and these are likely to reproduce annually, be shorter lived and reach maturity much more rapidly.

    Most of the characterizing species reproduce regularly but recruitment is often sporadic owing to interference competition with established adults of the same and other species. However, owing to the fact that the characterizing species take between 3 and 5 years to reach sexual maturity, it is likely that the time for the overall community to reach a fully diverse state will also be several years. It is likely that the low-energy hydrodynamic regime is an important factor in the maintenance of stable benthic populations in this biotope, as larvae are retained in the vicinity of the parent population.

    Importance review

    Policy/Legislation

    Habitats of Principal ImportanceMud habitats in deep water
    Habitats of Conservation ImportanceMud habitats in deep water
    UK Biodiversity Action Plan PriorityMud habitats in deep water
    Priority Marine Features (Scotland)Inshore deep mud with burrowing heart urchins

    Exploitation

    Nephrops norvegicus is the only species within the biotope that is of any commercial importance. Nephrops fisheries are of major economic importance and the species is fished in biotopes throughout its geographic range, including CMU.BriAchi. This includes both shallow semi-enclosed sea loch areas and offshore grounds in the Irish and North Seas. In British waters the Nephrops fishery has grown rapidly since its inception in the 1950s. Nephrops is now one of the most valuable fisheries in the north-eastern Atlantic (Hughes, 1998(b)). No other species in the biotope are commercially exploited.

    Additional information

    -

    Bibliography

    1. Anderson, S.J., Atkinson, R.J.A. & Tatlor, A.C., 1993. Behavioural and respiratory adaptations of the mud-burrowing shrimp Calocaris macandreae Bell (Thalassinidea, Crustacea) to the burrow environment. Ophelia, 34, 143-156.
    2. Atkinson, R.J.A., 1989. Baseline survey of the burrowing megafauna of Loch Sween, proposed Marine Nature Reserve, and an investigation of the effects of trawling on the benthic megafauna. Report to the Nature Conservancy Council, Peterborough, from the University Marine Biological Station, Millport, pp.1-59.
    3. Austen, M.C. & Widdicombe, S., 1998. Experimental evidence of effects of the heart urchin Brissopsis lyrifera on associated meiobenthic nematode communities. Journal of Experimental Marine Biology and Ecology, 222, 219-238.
    4. 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.
    5. Bailey, N., Howard, F.G. & Chapman, C.J., 1986. Clyde Nephrops: Biology and fisheries. Proceedings of the Royal Society of Edinburgh, 90 (B), 501-518.
    6. Ball, B., Munday, B. & Tuck, I., 2000b. Effects of otter trawling on the benthos and environment in muddy sediments. In: Effects of fishing on non-target species and habitats, (eds. Kaiser, M.J. & de Groot, S.J.), pp 69-82. Oxford: Blackwell Science.
    7. Bergman, M.J.N. & Hup, M., 1992. Direct effects of beam trawling on macro-fauna in a sandy sediment in the southern North Sea. ICES Journal of Marine Science, 49, 5-11.
    8. Bergman, M.J.N. & van Santbrink, J.W., 2000. Fishing mortality of populations of megafauna in sandy sediments. In The effects of fishing on non-target species and habitats (ed. M.J. Kaiser & S.J de Groot), 49-68. Oxford: Blackwell Science.
    9. Bradshaw, C., Veale, L.O., Hill, A.S. & Brand, A.R., 2000. The effects of scallop dredging on gravelly seabed communities. In: Effects of fishing on non-target species and habitats (ed. M.J. Kaiser & de S.J. Groot), pp. 83-104. Oxford: Blackwell Science.
    10. Bradshaw, C., Veale, L.O., Hill, A.S. & Brand, A.R., 2002. The role of scallop-dredge disturbance in long-term changes in Irish Sea benthic communities: a re-analysis of an historical dataset. Journal of Sea Research, 47, 161-184.
    11. Brattström, H., 1946. Observations on Brissopsis lyrifera (Forbes) in the Gullmar Fjord. Arkive fur Zoologie, 37A, 1-27.
    12. Buchanan, J.B. & Warwick, R.M., 1974. An estimate of benthic macrofaunal production in the offshore mud of the Northumberland coast. Journal of the Marine Biological Association of the United Kingdom, 54, 197-222.
    13. Buchanan, J.B., 1963. The biology of Calocaris macandreae ( Crustacea: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom, 43, 729-747.
    14. Buchanan, J.B., 1963(b). The bottom fauna communities and their sediment relationships off the coast of Northumberland. Oikos, 14, 154-175.
    15. Buchanan, J.B., 1965. Silt transportation and the distribution of macrobenthic animals off the Northumberland coast. Report of the Challenger Society, 3, 45.
    16. Buchanan, J.B., 1967. Dispersion and demography of some infaunal echinoderm populations. Symposia of the Zoological Society of London, 20, 1-11.
    17. Buchanan, J.B., 1974. A study of long term population stability in a benthic crustacean. Proceedings of the Challenger Society, 4, 252-253.
    18. Clyde River Purification Board, 1976. Monitoring in the Loch Fyne designated sea area. A survey in relation to the Stage III construction of a concrete gas production platform. Clyde River Purification Board, Technical Report No. 42., Unpublished.
    19. Connor, D.W., Dalkin, M.J., Hill, T.O., Holt, R.H.F. & Sanderson, W.G., 1997a. Marine biotope classification for Britain and Ireland. Vol. 2. Sublittoral biotopes. Joint Nature Conservation Committee, Peterborough, JNCC Report no. 230, Version 97.06., Joint Nature Conservation Committee, Peterborough, JNCC Report no. 230, Version 97.06.
    20. Conway Morris, S., 1995. A new phylum from the lobster's lips. Nature, 378, 661-662.
    21. 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.
    22. Crompton, T.R., 1997. Toxicants in the aqueous ecosystem. New York: John Wiley & Sons.
    23. Daan, R., Groenewould van het, H., Jong de, S.A. & Mulder, M., 1992. Physico-chemical and biological features of a drilling site in the North Sea, 1 year after discharges of oil-contaminated drill cuttings. Marine Ecology Progress Series, 91, 37-45.
    24. Dahllöf, I., Blanck, H., Hall, P.O.J. & Molander, S., 1999. Long term effects of tri-n-butyl-tin on the function of a marine sediment system. Marine Ecology Progress Series, 188, 1-11.
    25. 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.
    26. de Groot, S.J. & Apeldoorn, J., 1971. Some experiments on the influence of the beam trawl on the bottom fauna. International Council for the Exploration of the Sea (CM Papers and Reports) CM 1971/B:2, 5 pp. (mimeo).
    27. Eleftheriou, A. & Robertson, M.R., 1992. The effects of experimental scallop dredging on the fauna and physical environment of a shallow sandy community. Netherlands Journal of Sea Research, 30, 289-299.
    28. Eno, N.C., Clark, R.A. & Sanderson, W.G. (ed.) 1997. Non-native marine species in British waters: a review and directory. Peterborough: Joint Nature Conservation Committee.
    29. Fenaux, L., 1970. Maturation of the gonads and seasonal cycle of the planktonic larvae of the ophiuroid Amphiura chiajei Forbes. Biological Bulletin, 138, 262-271.
    30. Frid, C.L.J., Clark, R.A. & Hall, J.A., 1999. Long-term changes in the benthos on a heavily fished ground off the NE coast of England. Marine Ecology Progress Series, 188, 13-20.
    31. Graham, M., 1955. Effects of trawling on animals on the sea bed. Deep-Sea Research, 3 (Suppl.), 1-6.
    32. Gunnarsson, J.S. & Skold, M., 1999. Accumulation of polychlorinated biphenyls by the infaunal brittle stars Amphiura filiformis and A. chiajei: effects of eutrophication and selective feeding. Marine Ecology Progress Series, 186, 173-185.
    33. Hargrave, B.T., 1980. Factors affecting the flux of organic matter to sediments in a marine bay. In Marine Benthic Dynamics (eds. Tenore, K.R. & Coull, B.C.), 243-263. USA: University of South Carolina Press.
    34. Hill, A.E., Brown, J. & Fernand, L., 1997. The summer gyre in the western Irish Sea: shelf sea paradigms and management implications. Estuarine, Coastal and Shelf Science, 44, 83-95.
    35. Hill, T.O.; Emblow, C.S.; Northen, K.O., 1996. Marine Nature Conservation Review. Sector 6. Inlets in eastern England: area summaries. , Peterborough: Joint Nature Conservation Committee. [Coasts and Seas of the United Kingdom MNCR series.]
    36. Hiscock, K., 1983. Water movement. In Sublittoral ecology. The ecology of shallow sublittoral benthos (ed. R. Earll & D.G. Erwin), pp. 58-96. Oxford: Clarendon Press.
    37. Hiscock, K., ed. 1998. Marine Nature Conservation Review. Benthic marine ecosystems of Great Britain and the north-east Atlantic. Peterborough, Joint Nature Conservation Committee.
    38. Hollertz, K., 1998. The response of Brissopsis lyrifera (Echinoidea: Spatangoida) to organic matter on the sediment surface. In Echinoderm Research (eds. Candia Carnevali, M.D. & Bonasoro, F.), 79-84.
    39. Hollertz, K., Skold, M. & Rosenberg, R., 1998. Interactions between two deposit feeding echinoderms: the spatangoid Brissopsis lyrifera (Forbes) and the ophiuroid Amphiura chiajei (Forbes). Hydrobiologia, 376, 287-295.
    40. Holme, N.A., 1961. The bottom fauna of the English Channel. Journal of the Marine Biological Association of the United Kingdom, 41, 397-461.
    41. Holme, N.A., 1966. The bottom fauna of the English Channel. Part II. Journal of the Marine Biological Association of the United Kingdom, 46, 401-493.
    42. Houghton, R.G., Williams, T. & Blacker, R.W., 1971. Some effects of double beam trawling. International Council for the Exploration of the Sea CM 1971/B:5, 12 pp. (mimeo)., International Council for the Exploration of the Sea CM 1971/B:5, 12 pp. (mimeo).
    43. Howard, F. G., 1989. The Norway lobster. Scottish Fisheries Information Pamphlet No. 7. Second edition,, Department of Agriculture and Fisheries for Scotland.
    44. Hughes, D.J. & Atkinson, R.J.A., 1997. A towed video survey of megafaunal bioturbation in the north-eastern Irish Sea. Journal of the Marine Biological Association of the United Kingdom, 77, 635-653.
    45. Hughes, D.J., 1998b. Subtidal brittlestar beds. An overview of dynamics and sensitivity characteristics for conservation management of marine SACs. Natura 2000 report prepared for Scottish Association of Marine Science (SAMS) for the UK Marine SACs Project., Scottish Association for Marine Science. (UK Marine SACs Project, Vol. 3)., http://www.english-nature.org.uk/uk-marine
    46. Hutchins, D.A., Teyssié, J-L., Boisson, F., Fowler, S.W., & Fisher, N.S., 1996. Temperature effects on uptake and retention of contaminant radionuclides and trace metals by the brittle star Ophiothrix fragilis. Marine Environmental Research, 41, 363-378.
    47. Jones, N.S., 1951. The bottom fauna of the south of the Isle of Man. Journal of Animal Ecology, 20, 132-144.
    48. Kaiser, M.J. & Spencer, B.E., 1995. Survival of by-catch from a beam trawl. Marine Ecology Progress Series, 126, 31-38.
    49. Kashenko, S.D., 1994. Larval development of the heart urchin Echinocardium cordatum feeding on different macroalgae. Biologiya Morya, 20, 385-389.
    50. Keegan, B.F. & Mercer, J.P., 1986. An oceanographic survey of Killary Harbour on the west coast of Ireland. Proceedings of the Royal Irish Academy, 86B, 1-70.
    51. MacBride, E.W., 1914. Textbook of Embryology, Vol. I, Invertebrata. London: MacMillan & Co.
    52. Mackie, A.S.Y., Oliver, P.G. & Rees, E.I.S., 1995. Benthic biodiversity in the southern Irish Sea. Studies in Marine Biodiversity and Systematics from the National Museum of Wales. BIOMOR Reports, no. 1.
    53. McIntosh, W.C., 1975. The marine invertebrates and fishes of St. Andrews. Edinburgh.
    54. Munday, B.W. & Keegan, B.F., 1992. Population dynamics of Amphiura chiajei (Echinodermata: Ophiuroidea) in Killary Harbour on the west coast of Ireland. Marine Biology, 114, 595-605.
    55. Munday, B.W., 1993. Field survey of the occurrence and significance of regeneration in Amphiura chiajei (Echinodermata: Ophiuroidea) from Killary Harbour, west coast of Ireland. Marine Biology, 115, 661-668.
    56. Muus, K., 1981. Density and growth of juvenile Amphiura filiformis (Ophiuroidea) in the Oresund. Ophelia, 20, 153-168.
    57. Newton, L.C. & McKenzie, J.D., 1998. Brittlestars, biomarkers and Beryl: Assessing the toxicity of oil-based drill cuttings using laboratory, mesocosm and field studies. Chemistry and Ecology, 15, 143-155.
    58. Nilsson, H.C., 1999. Effects of hypoxia and organic enrichment on growth of the brittle star Amphiura filiformis (O.F. Müller) and Amphiura chaijei Forbes. Journal of Experimental Marine Biology and Ecology, 237, 11-30.
    59. Pagett, R.M., 1980. Tolerance to brackish water by ophiuroids with special reference to a Scottish sea loch, Loch Etive. In Echinoderms: Past and Present (ed. M. Jangoux), pp. 223-229. Rotterdam: Balkema.
    60. Pearson, T.H. & Rosenberg, R., 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology: an Annual Review, 16, 229-311.
    61. Petersen, C.G.J., 1918. The sea bottom and its production of fish food. A survey of the work done in connection with valuation of the Denmark waters from 1883-1917. Report of the Danish Biological Station, 25, 1-62.
    62. Peterson, C.H., 1977. Competitive organisation of the soft bottom macrobenthic communities of southern California lagoons. Marine Biology, 43, 343-359.
    63. Ramsay, K., Kaiser, M.J. & Hughes, R.N. 1998. The responses of benthic scavengers to fishing disturbance by towed gears in different habitats. Journal of Experimental Marine Biology and Ecology, 224, 73-89.
    64. Rauck, G., 1988. What influence have bottom trawls on the seafloor and bottom fauna? Informationen fur die Fischwirtschaft, Hamberg, 35, 104-106.
    65. Rosenberg, R. & Loo, L., 1988. Marine eutrophication induced oxygen deficiency: effects on soft bottom fauna, western Sweden. Ophelia, 29, 213-225.
    66. Rosenberg, R., Hellman, B. & Johansson, B., 1991. Hypoxic tolerance of marine benthic fauna. Marine Ecology Progress Series, 79, 127-131.
    67. Rowden, A.A., Jones, M.B. & Morris, A.W., 1998. The role of Callianassa subterranea (Montagu) (Thalassinidea) in sediment resuspension in the North Sea. Continental Shelf Research, 18, 1365-1380.
    68. Rygg, B., 1985. Effect of sediment copper on benthic fauna. Marine Ecology Progress Series, 25, 83-89.
    69. Schinner, G.O., 1993. Burrowing behaviour, substratum preference and distribution of Schisater canaliferus (Echinoidea: Spatangoida) in the Northern Adriatic Sea. Marine Ecology, 14, 129-145.
    70. Stickle, W.B. & Diehl, W.J., 1987. Effects of salinity on echinoderms. In Echinoderm Studies, Vol. 2 (ed. M. Jangoux & J.M. Lawrence), pp. 235-285. A.A. Balkema: Rotterdam.

    71. Suchanek, T.H., 1993. Oil impacts on marine invertebrate populations and communities. American Zoologist, 33, 510-523.
    72. Taylor, A.C., Field, R.H. & Parslow-Williams, P.J., 1996. The effects of Hematodinium sp. Infection on aspects of the respiratory physiology of the Norway lobster, Nephrops norvegicus. Journal of Experimental Marine Biology and Ecology, 207, 217-228.
    73. Tenore, K.R., 1998. Nitrogen in benthic food chains. In Nitrogen Cycling in Coastal Marine Environments, (eds. Blackburn, T.H. & Sörensen J.), 191-206. New York: John Wiley & Sons Ltd.
    74. Tuck, I.D., Atkinson, R.J.A. & Chapman, C.J., 1994. The structure and seasonal variability in the spatial distribution of Nephrops norvegicus burrows. Ophelia, 40, 13-25.
    75. Walsh, G.E., McLaughlin, L.L., Louie, M.K., Deans, C.H. & Lores, E.M., 1986. Inhibition of arm regeneration by Ophioderma brevispina (Echinodermata: Ophiuroidea) by tributyltin oxide and triphenyltin oxide. Ecotoxicology and Environmental Safety, 12, 95-100.
    76. Widdicombe, S. & Austen, M.C., 1998. Experimental evidence for the role of Brissopsis lyrifera (Forbes, 1841) as a critical species in the maintenance of benthic diversity and the modification of sediment chemistry. Journal of Experimental Marine Biology and Ecology, 228, 241-255.
    77. Widdicombe, S. & Austen, M.C., 1999. Mesocosm investigation into the effects of bioturbation on the diversity and structure of a subtidal macrobenthic community. Marine Ecology Progress Series, 189, 181-193.

    Citation

    This review can be cited as:

    Budd, G.C. 2004. Brissopsis lyrifera and Amphiura chiajei in circalittoral mud. In Tyler-Walters H. and Hiscock K. (eds) Marine Life Information Network: Biology and Sensitivity Key Information Reviews, [on-line]. Plymouth: Marine Biological Association of the United Kingdom. Available from: http://www.marlin.ac.uk/habitat/detail/139

    Last Updated: 27/10/2004