Hediste diversicolor and Macoma balthica in littoral sandy mud

20-10-2001
Researched byWill Rayment Refereed byThis information is not refereed.
EUNIS CodeA2.312 EUNIS NameHediste diversicolor and Macoma balthica in littoral sandy mud

Summary

UK and Ireland classification

EUNIS 2008A2.312Hediste diversicolor and Macoma balthica in littoral sandy mud
EUNIS 2006A2.312Hediste diversicolor and Macoma balthica in littoral sandy mud
JNCC 2004LS.LMu.MEst.HedMacHediste diversicolor and Macoma balthica in littoral sandy mud
1997 BiotopeLS.LMU.SMu.HedMacHediste diversicolor and Macoma balthica in sandy mud shores

Description

Littoral sandy mud and mud in sheltered, often estuarine, conditions with a community of polychaetes together with the bivalve Macoma balthica. The most abundant large polychaete is typically Hediste (Nereis) diversicolor, which can be readily seen when digging over the sediment. Other smaller polychaetes include Eteone longa, Nephtys hombergii, Aphelochaeta marioni, Pygospio elegans, Arenicola marina and Manayunkia aestuarina. Oligochaete worms (e.g. Tubificoides benedii, Tubificoides pseudogaster and enchytraeids) are common or abundant and the amphipod Corophium volutator may be abundant. The mud snail Hydrobia ulvae is often common, with individuals or their fine tracks visible on the mud surface. The bivalve Macoma balthica may be accompanied by Cerastoderma edule, Abra tenuis and Mya arenaria. The surface of the mud may be covered with green algae such as Ulva spp. or Ulva lactuca. There is usually a black anoxic layer close to the sediment surface. LMU.HedStr is a similar biotope that is associated with muddier sediment in reduced salinity conditions with Streblospio shrubsolii, Manayunkia aestuarina or Tharyx killariensis and with fewer bivalves. Three variations of this biotope are recognised: LMU.HedMac.Are, LMU.HedMac.Pyg and LMU.HedMac.Mare. (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

Recorded from estuaries all around mainland Britain. There are no records from Ireland although the biotope would be expected to occur here.

Depth range

Lower shore, Mid shore

Additional information

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Further information sources

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JNCC

Habitat review

Ecology

Ecological and functional relationships

  • The dominant and characterizing species in the biotope (Macoma balthica and Hediste diversicolor) are infaunal and display plasticity in their feeding methods (McLusky & Elliott, 1981; Nielsen et al., 1995). They are primarily deposit feeders but are able to switch to suspension feeding when conditions allow. For example, in the case of Hediste diversicolor, if phytoplankton concentrations are sufficiently high the species switches from predatory and surface deposit-feeding to suspension feeding. This behaviour is maintained as long as the phytoplankton concentration remains above a 'trigger level' of 1-3 µg chlorophyll a per litre (reviewed by Riisgard, 1994).
  • Obligate deposit feeders are also numerous in the biotope, e.g. Pygospio elegans, Aphelochaeta marioni, Arenicola marina and Hydrobia ulvae. Competition for resources is likely to occur between the deposit feeders. For example, densities of the amphipod, Corophium volutator, and the gastropod, Hydrobia ulvae, are strongly negatively correlated although the mechanism of the interaction is not well understood (Barnes & Hughes, 1992).
  • Furthermore, Corophium volutator and the infaunal annelid species in the biotope probably interfere strongly with each other. Adult worms probably reduce amphipod numbers by disturbing their burrows, while high densities of amphipods can prevent establishment of worms by consuming larvae and juveniles (Olafsson & Persson, 1986). Arenicola marina has been shown to have a strong negative effect on Corophium volutator due to reworking of sediment causing the amphipod to emigrate (Flach, 1992), and also on Pygospio elegans (Reise, 1985).
  • Suspension feeding bivalves , e.g. Cerastoderma edule, Mya arenaria and Abra tenuis, may occur where hydrodynamic conditions allow, i.e. in areas of stronger flow with coarser sediments.
  • Important epibenthic predators in the biotope include the shore crab, Carcinus maenas, and shrimps, e.g. Crangon crangon, which take infaunal populations of small bivalves, polychaetes and crustaceans (Elliot et al., 1998). Carcinus maenas has been shown to significantly reduce the numbers of Manayunkia aestuarina on mudflats (McClusky, 1989) and along with Crangon crangon may reduce the population of Corophium volutator in estuaries by more than 50% (Pihl, 1985).
  • Intertidal mudflats are important feeding areas for many fish species. The most significant predators are probably the flatfish, including sole, Solea solea, dab, Limanda limanda, flounder, Platichthys flesus, and plaice, Pleuronectes platessa, which feed on polychaetes and their tails (e.g. of Hediste diversicolor and Arenicola marina), bivalve young and siphons (e.g. of Macoma balthica) and crustaceans (see review by Elliot et al., 1998).
  • Mobile epibenthic predators are probably responsible for preventing the infauna reaching carrying capacity. For example, exclusion experiments by Reise (1985) on intertidal mudflats showed small fish and decapod crustaceans can significantly reduce numbers of Cerastoderma edule, Tubificoides benedii, Pygospio elegans, Aphelochaeta marioni, Eteone longa and Corophium volutator.
  • Carnivorous annelids, e.g. Eteone longa and Nephtys hombergii, operate at the trophic level below Carcinus maenas (Reise, 1985). They predate the smaller annelids and crustaceans in the biotope.
  • Macroalgae, such as Ulva lactuca and Ulva sp., probably only occur in the biotope where suitable hard substrata exist for attachment. However, Ulva lactuca may grow free floating in very sheltered conditions.

Seasonal and longer term change

Seasonal changes are likely to occur in the abundance of fauna in the biotope due to seasonal recruitment processes and variations in recruitment success. For example, in the case of Macoma balthica, Bonsdorff et al. (1995) reported juvenile density in the Baltic Sea following settlement in late summer to be 300,000/m² decreasing to a stable adult density of 1,000/m², and Ratcliffe et al. (1981) reported adult densities in the Humber Estuary, UK, between 5,000/m² and 40,000/m² depending on time since a successful spat fall. Variation in abundance is also very pronounced in the polychaete Aphelochaeta marioni. For example, in the Wadden Sea, peak abundance occurred in January (71,200 individuals per m²) and minimum abundance occurred in July (22,500 individuals per m²) following maximum spawning activity between May and July (Farke, 1979). However, the spawning period varies according to environmental conditions and so peak abundances will not necessarily occur at the same time each year. For example, Gibbs (1971) reported Aphelochaeta marioni spawning in late autumn in Stonehouse Pool, Plymouth Sound.
Some species make seasonal migrations in response to environmental conditions. For example, Beukema & De Vlas (1979) reported that 30% of the Macoma balthica population migrated into the subtidal during winter apparently in response to low temperatures. Migration is achieved by burrowing (Bonsdorff, 1984; Guenther, 1991) and/or floating (Sörlin, 1988) .
Macroalgal cover typically varies through the year due to changes in temperature and light availability. The green macroalgae in the biotope are likely to proliferate in the spring and summer and die back in the autumn and winter in conjunction with decreasing light levels and temperature and increased disturbance by storm events. Production by microphytobenthos and microalgae is also likely to be higher in spring and summer, increasing food availability for deposit feeders and suspension feeders in the biotope.
The biotope is likely to be susceptible to increased wave action during storms, particularly in winter. Storms may result in changes in sediment composition and washing out of infauna, leaving the biotope available for recolonization (see review by Hall, 1994). The infauna may be damaged by wave action, displaced from their preferred habitat and/or cast ashore, resulting in mortality. For example, Tamaki (1987) studied the passive transport by waves and tidal currents of the adults of 5 polychaete species. One species exhibited a landward shift in its centre of population during winter when the wave effects were most profound, and reoccupied its summer position by active migration of adults.

Habitat structure and complexity

  • The substratum in the biotope is uniform sediment with little structural diversity provided by either physiographic features or the biota. Some 3-dimensional structure is provided by the burrows of infauna such as Arenicola marina. Most species living within the sediment are limited to the area above the anoxic layer, the depth of which will vary depending on sediment particle size and organic content. However, the presence of burrows allows a larger surface area of sediment to become oxygenated, and thus enhances the survival of a considerable variety of small species (Pearson & Rosenberg, 1978).
  • Reworking of sediments by deposit feeders increases bioturbation and potentially causes a change in the substratum characteristics and the associated community (e.g. Rhoads & Young, 1970). For example, Widdows et al. (1998) reported that typical abundances of Macoma balthica increased sediment resuspension and/or erodability four fold and that there was a significant positive correlation between density of the species and sediment resuspension.
  • Where present, the macroalgae provide some structural complexity in the habitat, providing cover and sites for attachment of epifauna and epiphytes.

Productivity

  • Primary production in the biotope comes from benthic microalgae and water column phytoplankton (Elliott et al., 1998).
  • Production by benthic unicellular and filamentous algae in the littoral zone accounts for 0.2-1.3 g C/m² daily, depending on water clarity (Barnes & Hughes, 1992). Benthic microalgae are able to photosynthesize over a much wider range of light intensity than the planktonic species. There is little or no photoinhibition, adapting littoral species to the full sunlight experienced at low tide while still utilizing the very low light intensities at high tide (Barnes & Hughes, 1992).
  • Where present, macroalgae also contribute to primary production in the biotope. They exude considerable amounts of dissolved organic carbon which are taken up readily by bacteria and possibly by some larger invertebrates.
  • The majority of nutrients in the biotope are derived from allochthonous sources. Mudflats receive large inputs of nutrients, sediment and organic matter from the sea and land discharges of river water and sewage, resulting in high productivity despite low levels of primary production (Elliott et al., 1998).

Recruitment processes

The bivalves which characterize the biotope are capable of high recruitment and rapid recovery. For example, adult Macoma balthica spawn at least once a year and are highly fecund (Caddy, 1967). There is a planktotrophic larval phase which lasts up to 2 months (Fish & Fish, 1996) and so dispersal over long distances is potentially possible given a suitable hydrographic regime. Following settlement, development is rapid and sexual maturity is attained within 2 years (Gilbert, 1978; Harvey & Vincent, 1989). In addition to larval dispersal, dispersal of juveniles and adults occurs via burrowing (Bonsdorff, 1984; Guenther, 1991), floating (Sörlin, 1988) and probably via bedload transport (Emerson & Grant, 1991). It is expected therefore that recruitment can occur from both local and distant populations.
The infaunal polychaetes Hediste diversicolor, Arenicola marina and Aphelochaeta marioni have high fecundity and the eggs develop lecithotrophically within the sediment or at the sediment surface (Farke, 1979; Beukema & de Vlas, 1979). There is no pelagic larval phase and the juveniles disperse by burrowing. Recruitment must occur from local populations or by longer distance dispersal of postlarvae in water currents or during periods of bedload transport. For example, Davey & George (1986), found evidence that larvae of Hediste diversicolor were tidally dispersed within the Tamar Estuary over a distance of 3 km, as larvae were found on an intertidal mudflat which previously lacked a resident population of adults. Recruitment is therefore likely to be predictable if local populations exist but patchy and sporadic otherwise.
The deposit feeding gastropod Hydrobia ulvae appears to display plasticity in its developmental mechanism. Fish & Fish (1996) report planktotrophic development with a free-swimming larval phase lasting 3 weeks, while Pilkington (1971) stated that development occurred via a non-feeding benthic larvae which metamorphosed in just 3 days. It is possible that Hydrobia ulvae is able to change its developmental mechanism according to environmental conditions. If conditions are favourable, the eggs may hatch, develop directly and recruit locally. In more stressful conditions, it may benefit the individual to disperse its offspring more widely via a planktotrophic larva.
Recruitment of shallow burrowing infaunal species can depend on adult movement by bedload sediment transport and not just spat settlement and juvenile dispersal. Emerson & Grant (1991) investigated recruitment in Mya arenaria and found that bedload transport was positively correlated with clam transport. They concluded that clam transport at a high energy site accounted for large changes in clam density. Furthermore, clam transport was not restricted to storm events and the significance is not restricted to Mya arenaria recruitment. Many infauna, e.g. polychaetes, gastropods, nematodes and other bivalves, will be susceptible to movement of their substratum.

Time for community to reach maturity

No information was found concerning time taken for the community to reach maturity. However, the characterizing species are highly fecund and quick to grow and mature and so the community would be expected to reach maturity within 5 years.

Additional information

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Preferences & Distribution

Recorded distribution in Britain and IrelandRecorded from estuaries all around mainland Britain. There are no records from Ireland although the biotope would be expected to occur here.

Habitat preferences

Depth Range Lower shore, Mid shore
Water clarity preferences
Limiting Nutrients No information found
Salinity Full (30-40 psu), Variable (18-40 psu)
Physiographic Enclosed coast / Embayment
Biological Zone Eulittoral
Substratum Mud, Sandy mud
Tidal
Wave Extremely sheltered, Sheltered, Very sheltered
Other preferences

Additional Information

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

    Hediste diversicolor and Macoma balthica are both characteristic of the biotope and are important for its classification. Loss of either of these species from the biotope would result in loss of the biotope itself. However, the loss of either of the species would be unlikely to have significant knock-on effects for the rest of the community as other species exist which fulfil similar ecological roles. Hediste diversicolor and Macoma balthica are therefore defined as 'important characterizing' but not 'key'.
    Aphelochaeta marioni is a good example of the deposit feeding polychaetes in the biotope and is useful to consider when assessing biotope sensitivity. Similarly, Cerastoderma edule is a good example of the suspension feeding bivalves. Both species are therefore categorised as 'important other'.

    Species indicative of sensitivity

    Community ImportanceSpecies nameCommon Name
    Important otherAphelochaeta marioniA bristleworm
    Important otherCerastoderma eduleCommon cockle
    Important characterizingHediste diversicolorRagworm
    Important characterizingMacoma balthicaBaltic tellin

    Physical Pressures

     IntoleranceRecoverabilitySensitivitySpecies RichnessEvidence/Confidence
    High High Moderate Major decline High

    The majority of the species in the biotope are infaunal and would therefore be removed along with the substratum. This would result in loss of entire populations and therefore intolerance is assessed as high and species richness would experience a major decline. Recoverability is assessed as high (see additional information below).

    Low Very high Very Low Minor decline Moderate

    The important characterizing species in the biotope are infaunal and capable of burrowing. Smith (1955) noted that when a population of Hediste diversicolor was covered with several inches of sand, the worms burrowed through the additional material and showed no adverse reaction. Macoma balthicais also a mobile species and is able to burrow upwards and surface from a depth of 5-6 cm (Brafield & Newell, 1961; Brafield, 1963; Stekoll et al., 1980). It is possible that there would be an energetic cost related to the infauna relocating to their preferred depth and so intolerance is assessed as low. The energetic cost would be short lived so recoverability is assessed as very high. Ephemeral algae in the biotope would be smothered by a 5cm layer of sediment and therefore, where they were present beforehand there would be a minor decline in biotope species richness.

    Tolerant* Not relevant Not sensitive* Minor decline Low

    The dominant and characterizing species in the biotope (Macoma balthica and Hediste diversicolor) are infaunal and display plasticity in their feeding methods (McLusky & Elliott, 1981; Nielsen et al., 1995). They are primarily deposit feeders but are able to switch to suspension feeding when conditions allow. Neither species are therefore likely to be adversely affected by changes in siltation as they would be able to employ the feeding method most appropriate for the environmental conditions. An increase in suspended sediment would result in an increased rate of siltation and therefore an increased food supply for deposit feeders. The important characterizing species may therefore increase in abundance if food had been previously limiting. The species most likely to be adversely affected by an increase in suspended sediment are the obligate suspension feeders such as Cerastoderma edule and Mya arenaria. The feeding and respiration structures risk becoming clogged thus potentially impairing growth and reproduction (Grant & Thorpe, 1991; Navarro & Widdows, 1997). Increased siltation would also have a negative effect on macroalgae where present, by blocking out incident light. There may therefore be a minor decline in species richness in the biotope.

    Low Very high Moderate Minor decline High

    The majority of species in the biotope are either suspension feeders or deposit feeders and therefore rely on a supply of nutrients in the water column and at the sediment surface. A decrease in the suspended sediment would result in decreased food availability for suspension feeders. It would also result in a decreased rate of deposition on the substratum surface and therefore a reduction in food availability for deposit feeders. This would be likely to impair growth and reproduction. The benchmark states that this change would occur for one month and therefore would be unlikely to cause mortality. Furthermore, the dominant and characterizing species in the biotope (Macoma balthica and Hediste diversicolor) display plasticity in their feeding methods (McLusky & Elliott, 1981; Nielsen et al., 1995) and therefore are adapted to utilizing whatever food source is available. An intolerance of low is therefore recorded. When suspended sediment levels revert to their original levels, feeding activity would quickly return to normal and hence recoverability is recorded as very high.

    Low Very high Very Low No change Low

    The majority of the species in the biotope, including the important characterizing species, live infaunally in mud or muddy sand, a substratum with a high water content, and are therefore protected from desiccation stress. Additionally, most bivalves, including Macoma balthica, are able to respond to desiccation stress by valve adduction during periods of emersion, and most polychaetes are mobile enough to relocate if environmental conditions are stressful. However, during the period of emersion, the majority of species would not be able to feed and respiration would be compromised, so there is likely to be some energetic cost. Biotope intolerance is therefore recorded as low. Feeding and respiration would quickly return to normal when the biotope is reimmersed and so recoverability is recorded as very high. Although the bivalve, Mya arenaria, is unable to contain its siphons within its shell and therefore risks drying out, it lives deep in the sediment and can withdraw its siphons so that desiccation is not likely to be important.

    Low Very high Very Low No change Low

    The majority of the species in the biotope, including the important characterizing species, live infaunally in mud or muddy sand, and are therefore protected from the short term stresses of an increase in emergence regime. However, over time the increased emergence would be likely to result in an energetic cost due to reduced feeding opportunities. Many of the species in the biotope would be able to relocate to their preferred position on the shore. Macoma balthica, for example, is mobile and able to relocate in the intertidal by burrowing (Bonsdorff, 1984) or floating (Sörlin, 1988), and Hediste diversicolor is an active burrower, swimmer and crawler. No mortality of the important characterizing species is expected, but the energetic cost of lost feeding opportunities and relocation results in an intolerance assessment of low. The energetic cost would be quickly overcome when the emergence regime returns to normal so recoverability is assessed as very high. Less mobile species, such as the bivalves, Cerastoderma eduleand Mya arenaria, would be expected to suffer some mortality.

    Tolerant Not relevant Not sensitive* No change Low

    The biotope occurs on the lower shore and its characterizing species are all found in the shallow subtidal. Therefore, it is unlikely that the biotope would be intolerant of a decrease in emergence regime. Decreased emergence may allow the biotope to become established further up the shore, but not where the habitat is constrained by sea defences (Elliott et al., 1998).

    Intermediate High Low Decline Moderate

    The biotope occurs in areas such as estuaries (Connor et al., 1997b) where water flow rate is likely to be weak. An increase in water flow rate would change the sediment characteristics in which the biotope occurs, primarily by re-suspending and preventing deposition of finer particles (Hiscock, 1983). The underlying sediment in the biotope has a high mud content; a substratum which would be eroded in very strong tidal streams. Therefore, the infaunal species, such as Hediste diversicolor and Macoma balthica, would be outside their habitat preferences and some mortality would be likely to occur. For example, Green (1968) recorded that towards the mouth of an estuary where sediments became coarser and cleaner, Macoma balthica was replaced by another tellin species, Tellina tenuis. Additionally, the consequent lack of deposition of particulate matter at the sediment surface would reduce food availability for the deposit feeders in the biotope. The resultant energetic cost over one year would also be likely to result in some mortality. Species such as Macoma balthica and Hediste diversicolor, which are able to vary their feeding methods, may react to the change by switching to suspension feeding. A biotope intolerance of intermediate is recorded and species richness is expected to decline. Recoverability is assessed as high (see additional information below).

    Tolerant Not relevant Not sensitive* No change High

    The biotope occurs in areas such as estuaries (Connor et al., 1997b) where water flow rate is likely to be weak. The characterizing species thrive in low energy environments, are primarily deposit feeders and are capable of generating their own feeding and respiration currents. As a result of decreased water flow, rate of siltation is likely to increase, making conditions more favourable for deposit feeders. Indeed, Newell (1965) (cited in Green, 1968) noted that Macoma balthica populations in the Thames Estuary, UK, were denser where the grade of deposit was finer, possibly due to greater food availability. The biotope is therefore unlikely to be affected by a decrease in water flow rate.

    Low Very high Very Low Minor decline Very low

    The intolerance of the biotope to an increase in temperature is largely dependent on the sensitivities of the important characterizing species. Both Hediste diversicolor and Macoma balthica occur in southern Europe and therefore must be able to become acclimated to higher temperatures than experienced in Britain and Ireland. Furthermore, they live infaunally in sediment with a high water content and hence are insulated against temperature change. Oertzen (1969) recorded that Macoma balthica could tolerate temperatures up to 49°C before thermal numbing of gill cilia occurred presumably resulting in death. Ratcliffe et al. (1981) reported that Macoma balthica from the Humber Estuary, UK, tolerated 6 hours of exposure to temperatures up to 37.5°C with no mortality. It seems likely therefore that the species could adapt to a chronic change and tolerate a large acute change with no mortality. Bartels-Hardege & Zeeck (1990) demonstrated that sub-lethal temperature increases resulted in disruption of spawning in Hediste diversicolor, with potential adverse consequences on recruitment success. Despite, the apparent tolerance of the important characterizing species, there may be sublethal effects of temperature increase and biotope intolerance is assessed as low. These effects should be rapidly overcome when temperatures are restored to their original levels and so recoverability is assessed as very high. There is evidence that other species in the biotope are intolerant of temperature increase. For example, Sommer et al. (1997) reported a critical upper temperature of 20°C for Arenicola marina, above which the species resorts to anaerobic respiration, and noted that North Sea specimens could not acclimate to a 4°C increase above this temperature. For Cerastoderma edule, Wilson (1981) reported a median lethal temperature of 29°C for 96 hours exposure and along with Smaal et al. (1997) commented on the species' limited ability to acclimate to changes in temperature. An acute temperature increase may therefore result in a minor decline in species richness in the biotope.

    Tolerant Not relevant Not sensitive* Minor decline Moderate

    Both of the important characterizing species in the biotope appear to be very tolerant of low temperatures. Macoma balthica occurs in the Gulfs of Finland and Bothnia where the sea freezes for several months of the year (Green, 1968) and was apparently unaffected by the severe winter of 1962/3 which decimated populations of many other bivalve species (Crisp, 1964). Furthermore, De Wilde (1975) noted that Macoma balthica kept at 0°C maintained a high level of feeding activity. Hediste diversicolor was also apparently unaffected by the winter of 1962/63 (Crisp, 1964). The biotope is therefore assessed as 'not sensitive'. Other species in the biotope, however, are more intolerant of decreases in temperature, e.g. Cerastoderma edule and Arenicola marina, and there may be a minor decline in species richness.

    Low Very high Very Low Minor decline Low

    LMU.HedMac occurs in relatively turbid waters and therefore the species in the biotope are likely to be well adapted to turbid conditions. An increase in turbidity may affect primary production in the water column and therefore reduce the availability of diatom food, both for suspension feeders and deposit feeders. In addition, primary production by the microphytobenthos on the sediment surface may be reduced, further decreasing food availability for deposit feeders. However, primary production is probably not a major source of nutrient input into the system and, furthermore, phytoplankton will also immigrate from distant areas so the effect may be decreased. As the benchmark turbidity increase only persists for a year, decreased food availability would probably only affect growth and fecundity of the intolerant species so a biotope intolerance of low is recorded. As soon as light levels return to normal, primary production will increase and hence recoverability is recorded as very high. Where they occur, the macroalgae in the biotope are likely to be most affected by an increase in turbidity and may be eliminated, resulting in a minor decline in species richness.

    Tolerant Not relevant Not sensitive* No change Low

    A decrease in turbidity will mean more light is available for photosynthesis by macroalgae, phytoplankton in the water column and microphytobenthos on the sediment surface. This would increase the primary production in the biotope and may mean greater food availability for suspension feeders and deposit feeders. There may be a consequent proliferation of epifauna and macroalgae at the expense the previously dominant infauna. Macoma balthica and Hediste diversicolor may react to the proliferation of phytoplankton by switching to suspension feeding.

    Intermediate High Low Decline Low

    LMU.HedMac occurs in low energy environments categorized as 'sheltered' to 'extremely sheltered' on the wave exposure scale (Connor et al., 1997b). This suggests that the biotope would be intolerant of wave exposure to some degree. An increase in wave exposure by two categories for one year would be likely to affect the biotope in several ways. Fine sediments would be eroded (Hiscock, 1983) resulting in the likely reduction of the habitat of the infaunal species, e.g. Hediste diversicolor and Macoma balthica, and a decrease in food availability for deposit feeders. Strong wave action is likely to cause damage or withdrawal of delicate feeding and respiration structures of species within the biotope resulting in loss of feeding opportunities and compromised growth. Furthermore, species may be damaged or dislodged by scouring from sand and gravel mobilized by increased wave action. For example, Ratcliffe et al. (1981) reported that juvenile Macoma balthica are susceptible to displacement by water currents due to their small mass and inability to bury deeply. It is likely that some mortality would result and therefore an intolerance of intermediate is recorded. Recoverability is recorded as high (see additional information below). Macroalgae and species with delicate feeding structures, such as the polychaete Aphelochaeta marioni, are likely to be particularly vulnerable to increases in wave exposure and would probably be lost from the biotope completely. Species richness is therefore expected to decline.

    Tolerant Not relevant Not sensitive* No change High

    LMU.HedMac occurs in low energy environments categorized as 'sheltered' to 'extremely sheltered' on the wave exposure scale (Connor et al., 1997b). It is unlikely that a further decrease in wave exposure would have any appreciable effect on the biotope.

    Tolerant Not relevant Not relevant No change Low

    Macoma balthica is intolerant of shear-wave vibrations that propagate along the sediment surface in the frequency range 50-200 Hz (Franzen, 1995). When placed on the surface of the substratum and exposed to a shear-wave of typical velocity for unconsolidated muddy sand (15 m/s), the response of Macoma balthica consisted of frequent and intense digging attempts (Franzen, 1995). Species with feeding and respiration structures held at or above the sediment surface may respond to noise and vibration by withdrawing them. However, it is not expected that the biotope would be intolerant of noise or vibration at the level of the benchmark.

    Tolerant Not relevant Not relevant No change Low

    Hediste diversicolor demonstrates a distinct movement towards darkness (skototaxis) and it has been shown that feeding sensitises the worm to light and influences the response to a sudden increase in illumination (Herter, 1926; Evans, 1966; both cited in Clay 1967c). Similarly, Farke (1979) demonstrated that Aphelochaeta marioni responds to sudden illumination by retraction of palps and cirri and cessation of all activity for several minutes. However, it is unlikely that the species have the visual acuity to be adversely affected by the benchmark level of visual disturbance.

    Intermediate High Low No change Low

    The infaunal polychaetes in the biotope, including Hediste diversicolor, have a fragile hydrostatic skeleton, and are therefore vulnerable to damage by physical abrasion. An anchor dragging at the sediment surface may damage fragile feeding structures and/or penetrate the soft substratum sufficiently to impact the infauna. The bivalves in the biotope, although more robust, are also vulnerable to physical abrasion. For example, damage caused by mechanical harvesting has been reported in Cerastoderma edule (Pickett, 1973; Cotter et al., 1997). It is likely that some mortality would occur and therefore intolerance is assessed as intermediate, although species richness would be unlikely to decline. Recoverability is recorded as high (see additional information below).

    Intermediate High Low No change Moderate

    Macoma balthica is able to rebury itself within 17 minutes when placed on the surface of the substratum (McGreer, 1979). However, individuals displaced to the sediment surface are likely to suffer an increased risk of predation and some mortality may result. Hediste diversicolor is a rapid burrower, but, similarly, would experience an increased risk of predation. Intolerance is therefore assessed as intermediate. Recoverability is recorded as high (see additional information below).

    Chemical Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    High High Moderate Decline High

    Collier & Pinn (1998) investigated the effect on the benthos of ivermectin, a feed additive treatment for infestations of sea-lice on farmed salmonids. Hediste diversicolor was particularly susceptible, exhibiting 100% mortality within 14 days when exposed to 8 mg/m² of ivermectin in a microcosm. For reference, Davies et al. (1998) reported that beneath a salmon farm, ivermectin may reach the seabed at concentrations between 2.2 and 6.6 mg/m². Arenicola marina was also intolerant of ivermectin through the ingestion of contaminated sediment (Thain et al., 1998; cited in Collier & Pinn, 1998) and it was suggested that deposit feeding was an important route for exposure to toxins. Beaumont et al. (1989) investigated the effects of tri-butyl tin (TBT), the toxic component of many antifouling paints, on benthic organisms. At concentrations of 1-3 µg/l there was no significant effect on the abundance of Hediste diversicolor after 9 weeks in a microcosm. However, no juvenile polychaetes were retrieved from the substratum and hence there is some evidence that TBT had an effect on the larval and/or juvenile stages.
    Beaumont et al. (1989) concluded that bivalves are particularly intolerant of tri-butyl tin (TBT). For example, when exposed to 1-3 µg TBT/l, Cerastoderma edule suffered 100% mortality after 2 weeks. There is also evidence that TBT causes recruitment failure in bivalves, either due to reproductive failure or larval mortality (Bryan & Gibbs, 1991). Little evidence was found concerning the effects of synthetic chemicals specifically on Macoma balthica. Bryan & Gibbs (1991) recorded bioaccumulation of TBT by Macoma balthica to be similar to Cerastoderma edule and Duinker et al. (1983) recorded bioaccumulation of polychlorinated bi-phenyls (PCBs) by Macoma balthica but made no comment on toxicity to the species.
    The evidence suggests that synthetic chemicals are toxic to the benthos generally and specifically to Hediste diversicolor and bivalves. High mortality is likely to result if the biotope is exposed to synthetic chemicals and so intolerance is assessed as high and species richness is expected to decline. Recoverability is recorded as high (see additional information below).

    Heavy metal contamination
    High High Moderate Decline High

    The bivalves in the biotope are particularly intolerant of heavy metal contamination. For Macoma balthica, lethal and sublethal effects have been reported caused by exposure to Cu, Pb, Zn, Cr, Ag, Hg, Cd and Fe (McGreer, 1979; Luoma et al., 1983; Boisson et al., 1998). For example, Luoma et al. (1983) investigated the intolerance of Macoma balthica from different populations within San Francisco Bay to copper, in the form of seawater spiked with copper sulphate. The 10 day LC50 varied between 210 µg/l and 1290 µg/l. They suggested that physiological and/or genetic adaptations could be responsible for the heterogeneity of the sensitivities and added that species survival depends more on the range of adaptive capacity within the species rather than identification of a single value of lethal or sublethal toxicant concentration. For reference, the lethal copper concentrations reported by Luoma et al. (1983) are similar to copper concentrations in freshwater inputs to the Fal Estuary, UK, reported by Bryan & Gibbs (1983). They reported that transplantation of Cerastoderma edule into Restronguet Creek resulted in 10-15% mortality within 63 days and 100% within 4 months.
    Generally, polychaetes (e.g. Bryan, 1984), gastropods (e.g. Bryan, 1984) and macroalgae (e.g. Strömgren, 1979a,b) are regarded as being tolerant of heavy metal contamination. In light of the high intolerance of bivalves, including the important characterizing species, overall biotope intolerance is assessed as high and species richness is expected to decline. Recoverability is recorded as high (see additional information below).

    Hydrocarbon contamination
    High High Moderate Major decline High

    Oil spills resulting from tanker accidents can cause large-scale deterioration of communities in shallow sedimentary systems. The majority of benthic species often suffer high mortality, allowing a few tolerant opportunistic species to proliferate. For example, after the Florida spill of 1969 in Massachusetts, the entire benthic fauna was eradicated immediately following the spill and populations of the opportunistic polychaete Capitella capitata increased to abundances of over 200,000/m² (Sanders, 1978). Similarly, the 1969 West Falmouth Spill of Grade 2 diesel fuel eradicated the entire benthic fauna, including Hediste diversicolor, and continued to have an impact more than a year after the spill due to remobilization of the oil (Suchanek, 1993).
    Suchanek (1993) reviewed the effects of oil on bivalves. Sublethal concentrations may produce substantially reduced feeding rates and/or food detection ability, probably due to ciliary inhibition. Respiration rates have increased at low concentrations and decreased at high concentrations. Generally, contact with oil causes an increase in energy expenditure and a decrease in feeding rate, resulting in less energy available for growth and reproduction. Sublethal concentrations of hydrocarbons also reduce byssal thread production (thus weakening attachment) and infaunal burrowing rates. Mortality following oil spills has been recorded in Macoma balthica (Stekoll et al., 1980), Mya arenaria (Dow, 1978; Johnston, 1984) and Cerastoderma edule (SEEEC, 1998). Suchanek (1993) reported that infaunal polychaetes were also vulnerable to hydrocarbon contamination. For example, high mortality has been demonstrated in Arenicola marina (Levell, 1976). However, deposit feeders, such as Aphelochaeta marioni, are likely to be less vulnerable due to the feeding tentacles being covered with a heavy secretion of mucus (Suchanek, 1993).
    The evidence suggests that oil spills have the potential to result in high mortality of many of the species in the biotope, including the important characterizing ones, and so biotope intolerance is assessed as high with a major decline in species richness. Recoverability is recorded as high (see additional information below) but will depend upon the persistence of hydrocarbons in the sediment.

    Radionuclide contamination
    No information Not relevant No information Insufficient
    information
    Not relevant

    Beasley & Fowler (1976) and Germain et al. (1984) examined the accumulation and transfers of radionuclides in Hediste diversicolor from sediments contaminated with americium and plutonium derived from nuclear weapons testing and the release of liquid effluent from a nuclear processing plant. Both concluded that the uptake of radionuclides by Hediste diversicolor was small. Beasley & Fowler (1976) found that Hediste diversicolor accumulated only 0.05% of the concentration of radionuclides found in the sediment. Hutchins et al. (1998) described the effect of temperature on bioaccumulation by Macoma balthica of radioactive americium, caesium and cobalt, but made no comment on the intolerance of the species. The biological significance of these findings is not clear and so an intolerance assessment has not been attempted.

    Changes in nutrient levels
    Intermediate High Low Decline Moderate

    Nutrient enrichment can lead to significant shifts in community composition in sedimentary habitats. Typically the community moves towards one dominated by deposit feeders and detritivores, such as polychaete worms (see review by Pearson & Rosenberg, 1978). The biotope includes species tolerant of nutrient enrichment and typical of enriched habitats (e.g. Tubificoides sp.) (Pearson & Rosenberg, 1978). It is likely that such species would increase in community importance following nutrient enrichment, with an associated decline in suspension feeding bivalves such as Cerastoderma edule and Mya arenaria.
    It has been suggested that Macoma balthica has the potential to be used as an indicator organism of organic pollution (Pearson & Rosenberg, 1978; Pekkarinen, 1983; Mölsa, 1986), as the species was reported to increase in abundance towards the sources of nutrient enrichment and to disappear when the organic loading became heavier (Anger, 1975 a & b; Landner et al., 1977). Madsen & Jensen (1987) reported the population of Macoma balthica to increase in abundance and biomass at two localities in the Danish Wadden Sea experiencing nutrient enrichment caused by a waste water discharge.
    A study by Norkko & Bonsdorff (1996) revealed the community effects of nutrient enrichment. Artificially constructed algal mats were anchored on a medium to fine sand substratum with an infauna dominated by Macoma balthica, Hydrobia sp., Pygospio elegans, Manayunkia aestuarina, Nereis diversicolor and oligochaetes. After 34 days the temperature underneath the mats was higher than in the free bottom water (13.0°C vs. 11.5°C) and the oxygen concentration in the water had decreased from 10 mg/l to less than 2 mg/l. Initially there was an increase in species numbers, abundance and biomass under the mats, suggesting that the infauna benefited from the additional food supply. However, after 16 days, all 3 measures had significantly declined. Macoma balthica density decreased from 1250/m² at day 0 to 96/m² at day 29, with some emigrating into the algae but many dying at the sediment surface. There were also significant reductions in abundance of Hydrobia sp., Pygospio elegans and Manayunkia aestuarina. Nereis diversicolor and the oligochaetes, however, tolerated the nutrient enriched and hypoxic conditions and therefore increased dramatically in community importance. Following removal of the algal mats, the species to recover most quickly were the Hydrobia sp., which were dominant in the surrounding unimpacted benthos and highly mobile.
    The intolerance of the biotope is therefore dependent on the level of nutrient enrichment. Initially, the deposit feeders in the biotope are likely to proliferate at the expense of the suspension feeders. However, in extreme cases of enrichment and associated hypoxia, mass mortality may result and tolerant species such as oligochaetes and Hediste diversicolor may proliferate. Intolerance is therefore assessed as intermediate with a decline in species richness. Recoverability is recorded as high (see additional information below).

    Tolerant Not relevant Not relevant No change High

    The biotope occurs in fully saline conditions (Connor et al., 1997b) so is unlikely to be affected by increases in salinity. The reaction of a number of species to hypersaline conditions (>40 psu) has been studied. McLusky & Allan (1976) reported that Macoma balthica failed to grow at 41 psu. Rygg (1970) noted that a population of Cerastoderma edule did not survive 23 days exposure at 60 psu, although they did survive at 46 psu. When exposed to hyper-osmotic shock (47 psu), Arenicola marina lost weight, but were able to regulate and gain weight within 7-10 days (Zebe & Schiedek, 1996).

    Low Very high Moderate Minor decline High

    The biotope often occurs in areas of variable salinity in estuaries (Connor et al., 1997b) and hence the characterizing species are likely to experience large changes in salinity. The benchmark decrease would place a portion of the biotope in "reduced" salinity conditions (<18 psu). The sensitivities of the important characterizing species are the most important to consider when assessing the intolerance of the biotope. Hediste diversicolor is a euryhaline species, able to tolerate salinities down to 5 psu or less (Barnes, 1994). However, low salinities (< 8 psu) can have an adverse effect on reproduction (Ozoh & Jones, 1990; Smith 1964). McLusky & Allan (1976) conducted salinity survival experiments with Macoma balthica over a period of 150 days. At 12 psu specimens survived 78 days, whilst specimens at 8.5 psu survived 40 days. Some specimens of Macoma balthica survived 2.5 days at 0.8 psu, which was apparently due to the animals ability to clamp its valves shut in adverse conditions. McLusky & Allan (1976) also reported that Macoma balthica failed to grow (increase shell length) at 15 psu. Hence it would seem that although reduced salinity would not result in mortality of the important characterizing species, growth and reproduction would be compromised and so intolerance is assessed as low. Other species in the biotope are less tolerant of reduced salinity. Arenicola marina, for example, is unable to tolerate salinities below 24 psu and is excluded from areas influenced by freshwater runoff or input (e.g. the head end of estuaries) (Hayward, 1994). There may therefore be a minor decline in species richness.

    Low Very high Very Low Minor decline High

    The biotope often has a black anoxic layer close to the sediment surface, so the characterizing species are likely to be tolerant of reduced oxygen conditions. The important characterizing species in the biotope are very tolerant of hypoxia. Dries & Theede (1974) reported the following LT50 values for Macoma balthica maintained in anoxic conditions : 50 - 70 days at 5°C, 30 days at 10°C, 25 days at 15°C and 11 days at 20°C. Theede (1984) reported that the ability of Macoma balthica to resist extreme oxygen deficiency was mainly due to cellular mechanisms. Of considerable importance are sufficient accumulations of reserve compounds, e.g. glycogen, and the ability to reduce energy requirements for maintenance of life by reducing overall activity (Theede, 1984). Vismann (1990) reported that Hediste diversicolor endured 22 days of exposure to oxygen concentrations of 2.8 mg/l with only 15% mortality. Both species have been observed to respond to hypoxic sediments by emigration (Brafield & Newell, 1961; Vismann, 1990). The benchmark change in oxygenation is 2 mg/l for a week. Both Hediste diversicolor and Macoma balthica would be expected to tolerate this change, although growth and reproduction would probably be compromised during this period. Biotope intolerance is therefore assessed as low. Metabolic activity should quickly return to normal when normoxia resumes so recoverability is recorded as very high. Other species in the biotope are less tolerant of hypoxia. For example, Cerastoderma edule suffered 50% mortality after 4.25 days at 1.5 ml O2/l (Theede et al., 1969). There may therefore be a minor decline in species richness.

    Biological Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    Intermediate High Low No change Low

    Hediste diversicolor is parasitized by the coccidian, Coelotropha durchoni, but apparently does not suffer mortality (Porchet-Hennere & Dugimont, 1992). Macoma balthica is parasitized by Lacunovermis macomae (Lebour) and the trematode, Parvatrema affinis which is known to cause sexual castration (Swennen & Ching, 1974). Some mortality is therefore likely and intolerance is assessed as intermediate. Recoverability is recorded as high (see additional information below).

    No information Not relevant No information Insufficient
    information
    Not relevant

    There is no evidence to suggest that the biotope may be colonized by non-native species.

    Intermediate High Low Minor decline Very low

    Hediste diversicolor is extracted by bait diggers (Anon, 1999). However, very little information was found concerning the effect of this extraction and it is not possible to assess biotope intolerance further than saying that a proportion of the target species would be removed. In general, bait harvesting may have a negative effect on intertidal benthic habitats. For example, mechanical harvesting for Arenicola marina resulted in drastic reduction in the population of Mya arenaria in the Wadden Sea (Beukema, 1995), and commercial digging of mudflats in Maine, USA, reduced total number of infaunal taxa (Brown & Wilson, 1997).

    Intolerance has been assessed as intermediate to reflect the likelihood that various species will experience some loss. Recoverability is assessed as high (see additional information below).

    Not relevant Not relevant Not relevant Not relevant Not relevant

    Additional information

    Recoverability
    The recoverability of the biotope is largely dependent on the recoverability of the important characterizing species.
    The polychaete Hediste diversicolor has high fecundity and the eggs develop lecithotrophically within the burrow, brooded by the female (Fish & Fish, 1996). There is no pelagic larval phase and the juveniles disperse principally by burrowing. Recolonization of disturbed sediments must therefore occur by immigration from local populations of juveniles or adults or by longer distance dispersal of postlarvae in water currents or during periods of bedload transport. For example, Davey & George (1986), found evidence that larvae of Hediste diversicolor were tidally dispersed within the Tamar Estuary over a distance of 3 km, as larvae were found on an intertidal mudflat which previously lacked a resident population of adults. Recovery is therefore likely to be rapid and predictable if local populations exist but slow and sporadic otherwise. It is probable that, in the majority of cases, recovery would occur within 5 years and so species recoverability is assessed as high. Other infaunal deposit feeding polychaetes in the biotope such as Arenicola marina and Aphelochaeta marioni display similar recoverability characteristics.
    The life history characteristics of Macoma balthica give the species strong powers of recoverability. Adults spawn at least once a year and are highly fecund (Caddy, 1967). There is a planktotrophic larval phase which lasts up to 2 months (Fish & Fish, 1996) and so dispersal over long distances is potentially possible given a suitable hydrographic regime. Following settlement, development is rapid and sexual maturity is attained within 2 years (Gilbert, 1978; Harvey & Vincent, 1989). In addition to larval dispersal, dispersal of juveniles and adults occurs via burrowing (Bonsdorff, 1984; Guenther, 1991), floating (Sörlin, 1988) and probably via bedload transport (Emerson & Grant, 1991). It is expected therefore that recruitment can occur from both local and distant populations. Bonsdorff (1984) studied the recovery of a Macoma balthica population in a shallow, brackish bay in SW Finland following removal of the substratum by dredging in the summer of 1976. Recolonization of the dredged area by Macoma balthica began immediately after the disturbance to the sediment and by November 1976 the Macoma balthica population had recovered to 51 individuals/m². One year later there was no detectable difference in the Macoma balthica population between the recently dredged area and a reference area elsewhere in the bay. In 1976, 2 generations could be detected in the newly established population indicating that active immigration of adults was occurring in parallel to larval settlement. In 1977, up to 6 generations were identified, giving further evidence of active immigration to the dredged area. In light of the life history characteristics of Macoma balthica and the evidence of recovery, recoverability of the species is assessed as high.
    Norkko & Bonsdorff (1996) studied the recoverability of a community in the Baltic Sea very similar to that which occurs in the LMU.HedMac biotope. Artificial algal mats were anchored on the substratum which resulted in significant declines in infaunal species richness, abundance and biomass due to induced organic enrichment and hypoxia. They found that recolonization of the impacted area over the 5 days from when the impact source was removed was quickest by the gastropod Hydrobia sp., the species which dominated the faunal community of the surrounding area. Short term recoverability, therefore, is likely to be determined by proximity of source populations and species mobility.
    In view of the recoverability of the characterizing species, the overall recoverability of the biotope is assessed as high. However, in situations where the biotope is locally perturbed but unimpacted areas persist, there is the potential for the affected areas to recover very quickly due to immigration of mature individuals.

    Importance review

    Policy/Legislation

    Habitats of Principal ImportanceIntertidal mudflats
    Habitats Directive Annex 1Mudflats and sandflats not covered by seawater at low tide, Estuaries
    UK Biodiversity Action Plan PriorityIntertidal mudflats
    OSPAR Annex VIntertidal mudflats
    Priority Marine Features (Scotland)Intertidal mudflats

    Exploitation

    The biotope is exploited by bait diggers (Anon, 1999), the principal target species being the polychaetes, Hediste diversicolor and Arenicola marina.
    There are also likely to be commercial fisheries for bivalve species, e.g. Cerastoderma edule (Hall & Harding, 1997), and shrimps (Anon, 1999).
    The biotope is at risk from land reclamation. For example, land claim for urban infrastructure and industry has removed approximately 25% of Great Britain's estuarine intertidal flats (Anon, 1999).

    Additional information

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    Citation

    This review can be cited as:

    Rayment, W.J. 2001. Hediste diversicolor and Macoma balthica in littoral sandy 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/209

    Last Updated: 20/10/2001