Source: https://www.marlin.ac.uk/habitats/detail/331
Timestamp: 2019-04-25 08:44:25+00:00

Document:
Researched by Dr Heidi Tillin & Dr Matt Ashley Refereed by This information is not refereed.
Mainly mid shore mud or sandy mud subject to variable salinity on sheltered estuarine shores. Typically, the sediment is wet in appearance and has an anoxic layer below 1 cm depth. The surface of the mud has the distinctive 'crow's foot' pattern formed by the peppery furrow shell Scrobicularia plana. The infauna is additionally characterised by a range of polychaete and bivalve species, including the ragworm Hediste diversicolor, Pygospio elegans, Streblospio shrubsolii, Tharyx killariensis and the baltic tellin Limecola balthica. Oligochaetes, most notably Tubificoides benedii, and the spire shell Hydrobia ulvae may be abundant. Other species that sometimes occur in this biotope are the cockle Cerastoderma edule, the sand gaper Mya arenaria and the polychaetes Eteone longa and Nephtys hombergii. HedMacScr may occur on the same shores as NhomLimStr, HedMac, NhomAph, Hed.Str and Hed.Cvol. Higher up on the shore, and/or further towards the head of the estuary, Hed.Ol may occur, changing to Tben at the upper extreme of the estuary. Ulva spp. may form mats on the surface of the mud during the summer months, particularly in areas of nutrient enrichment. (Infromation from Connor et al., 2004; JNCC, 2015).
The biotope is characterized by the ragworm Hediste diversicolor (JNCC, 2015) and the sensitivity assessments, therefore, focus on this species. The surface of the mud has the distinctive 'crow's foot' pattern formed by the peppery furrow shell Scrobicularia plana and this species is considered in the sensitivity assessments. The infauna is additionally characterized by a range of polychaete and bivalve species, including the ragworm Hediste diversicolor, Pygospio elegans, Streblospio shrubsolii and the Baltic tellin Limecola balthica. Oligochaetes, most notably Tubificoides benedii, and the spire shell Hydrobia ulvae may be abundant and the sensitivity of these species is considered.
When impacted this biotope may recover through repair of damaged individuals, adult migration by mobile species and recolonization by pelagic larvae. The ability of postlarvae, larger juveniles, and adults of the key characterizing species Hediste diversicolor to swim, burrow and be carried by bedload transport can aid the rapid recolonization of disturbed sediments (Shull, 1997). Davey & George (1986), found evidence that larvae of Hediste diversicolor were tidally dispersed within the Tamar Estuary over a distance of 3 km. Such passive dispersal alone suggested that recolonization of disturbed sediments, or populations removed from bait digging was likely to occur rapidly, depending upon larvae transport pathways.
Generally Hediste diversicolor is reported to reach maturity between one and three years of age, like other Nereidae, Hediste diversicolor are monotelic, that is, they reproduce only once in their lifetime and then die (Olive & Garwood, 1981). Populations appear to show local characteristics in terms of spawning periods. Spawning may be limited to a short period in spring or extend over the summer. In the Thames Estuary, Dales (1950) reported specimens growing to maturity within one year, spawning in February, with some individuals surviving up to 18 months. Mettam et al. (1982), reported that Hediste diversicolor from the Severn Estuary matured rapidly in the spring and spawned at two years old. Olive & Garwood (1981), found that females in the Blyth Estuary, Northumberland, were in their second year before eggs began to appear, so most probably spawned in their third year.
Mature males crawl around outside in search of a mature female and discharge sperm through the nephridia, directly outside her burrow. Direct contact between the sexes is not a necessity. Sperm is drawn into the burrow by females and fertilized eggs remain inside the burrow protected by the female. Both sexes die shortly after spawning. The trait to lay and protect eggs within a burrow is likely to increase the time populations recover from pressures such as sediment removal, as both adults and eggs will be affected. The pelagic larval dispersal phase is short (Scaps, 2002).
In general, recovery of Hediste diversicolor populations from impacts appears to be relatively rapid. Recovery will be enhanced where adult migration (active or passive) can transport adults from adjacent, unimpacted habitats. Where a large area is severely impacted, however, recovery may require longer time-scales. The effects of a pipeline construction on benthic invertebrates were investigated using a Before/After impact protocol at Clonakilty Bay, West Cork, Ireland. Benthic invertebrates were sampled once before the excavation and at one, two, three and six months after the completion of the work.. An impact was obvious in the construction site in that no live invertebrates were found at one month after disturbance, but there followed a gradual recolonization by Hediste diversicolor. At six months after the disturbance, there was no significant difference in the mean number of total individuals (of all species) per core sample amongst all study sites, but the apparent recovery in the impacted area was due to recovery of Hediste diversicolor and Tubifex spp. (Lewis et al., 2002b).
Bolam et al. (2004) experimentally simulated (in the field) the effect of dredged material emplacement (beach recharge) by manipulating defaunated sediments. Macrofaunal sampling was carried out after 1 week and after 1, 3, 6 and 12 months. Recolonization patterns, although gradual, were found to be species specific with abundances of the polychaete Hediste diversicolor and the gastropod Hydrobia ulvae recovering to ambient levels within one week.
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). Females are capable of producing 10,000-30,000 eggs (MES, 2010). 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 Limecola balthica (as Macoma balthica) population in a shallow, brackish bay in SW Finland following the removal of the substratum by dredging in the summer of 1976. Recolonization of the dredged area by Limecola balthica began immediately after the disturbance to the sediment and by November 1976, the Limecola balthica population had recovered to 51 individuals/m². One year later there was no detectable difference in the Limecola balthica population between the recently dredged area and a reference area elsewhere in the bay. In 1976, two 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 six generations were identified, giving further evidence of active immigration to the dredged area.
The polychaete Pygospio elegans have life history strategies that allow rapid colonization and population increase in disturbed and defaunated patches where there is little competition from other species. Pygospio elegans exhibit a number of reproductive strategies (a trait known as poecilogony). Larvae may develop directly allowing rapid population increase in suitable patches or they may have a planktonic stage (allowing colonization of new habitats). Experimental defaunation studies have shown an increase in Pygospio elegans, higher than background abundances within 2 months, reaching maximum abundance within 100 days (Van Colen et al. 2008). Following a period of anoxia in the Bay of Somme (north France) that removed cockles, Pygospio elegans increased rapidly but then decreased as cockle abundance recovered and sediments were disturbed by cockle movement (Desprez et al., 1992). Re-colonization of Pygospio elegans, was observed in 2 weeks by Dittmann et al. (1999) following a 1 month long defaunation of the sediment. However, McLusky et al. (1983) found that Pygospio elegans were significantly depleted for >100 days after harvesting (surpassing the study monitoring timeline). Ferns et al. (2000) found that tractor-towed cockle harvesting removed 83% of Pygospio elegans (initial density 1850 per m2). In muddy sand habitats, Pygospio elegans had not recovered their original abundance after 174 days (Ferns et al., 2000). These results are supported by work by Moore (1991) who also found that cockle dredging can result in reduced densities of some polychaete species, including Pygospio elegans. Rostron (1995) undertook experimental dredging of sandflats with a mechanical cockle dredger, including a site comprised of stable, poorly sorted fine sands with small pools and Arenicola marina casts with some algal growths. At this site, post-dredging, there was a decreased number of Pygospio elegans with no recovery to pre-dredging numbers after six months.
Tubificid populations tend to be large and to be constant throughout the year, although some studies have noticed seasonal variations (Giere & Pfannkuche, 1982). Many species, including Tubificoides benedii andBaltidrilus costata have a two-year reproductive cycle and only part of the population reproduces each season (Giere & Pfannkuche, 1982). Populations of Tubificoides benedii in the Fourth estuary have not demonstrated clear seasonality in recruitment (Bagheri & McLusky, 1982), although mature Tubificoides benedii (as Peloscolex benedeni) in the Thames Estuary were reported to occur in December with a maximum in late February (Hunter & Arthur, 1978), breeding worms increased from April and maximum cocoon deposition was observed in July (Hunter & Arthur, 1978). Bolam and Whomersley (2003) observed faunal recolonization of fine sediments placed on saltmarsh as a beneficial use and disposal of fine grained dredged sediments. They found that tubificid oligochaetes began colonizing sediments from the first week following a beneficial use scheme involving the placement of fine-grained dredged material on a salt marsh in southeast England. The abundance of Tubificoides benedii recovered slowly in the recharge stations and required 18 months to match reference sites and those in the recharge stations prior to placement of sediments. The results indicate that some post-juvenile immigration is possible and that an in-situ recovery of abundance is likely to require more than 1 year. Rapid recolonization has also been observed in the tubificid oligochaete Baltidrilus costata (Tubifex costatus) appeared in upper sediment layers in experimentally defaunated patches (4m2) after 3 weeks (Gamenick et al., 1996).
Resilience assessment. Resilience is assessed as ‘High’ (within 2 years), where resistance is ‘High’, ‘Medium’ or ‘Low’ based on Bolam et al. (2004), Bolam & Whomersley, (2003), Bonsdorff (1984), and Gamenick et al. (1996). Resilience is assessed as ‘Medium’ (2-10 years) where, resistance is ‘None’ and habitat recovery may also be required.
Hediste diversicolor and other important characterizing species are adapted to living within the intertidal zone where temperatures fluctuate. Some resistance to temperature fluctuations is achieved by burying within the sediment, which buffers against acute temperature changes over the tidal cycle.
The geographic range of Hediste diversicolor (throughout north-west Europe on the Baltic Sea, North Sea and along Atlantic coasts to the Mediterranean) suggests that it is tolerant of a range of temperatures and a temperature increase at benchmark levels is unlikely to have an adverse effect on UK populations. Hediste diversicolor can tolerate temperatures from below zero under Baltic ice to high summer temperatures in Black Sea lagoons (>25°C) (Smith, 1977).
Hediste diversicolor were not strongly affected by heat waves in an estuary in north western Portugal, where temperatures reached 40°C in intertidal pools (higher temperatures than experienced around UK and Irish coasts) (Dolbeth et al., 2011). Grilo et al., 2011) found that, at a Portuguese site, surface deposit feeders gradually decreased in periods of higher temperatures. However, sub-surface deposit feeders became dominant for up to 3 years after heat wave conditions had passed.
Temperature change may adversely affect reproduction. Bartels-Hardege and Zeeck (1990) demonstrated that an increase from 12°C and maintenance of water temperature at 16°C induced reproduction in Hediste diversicolor specimens outside the normal period of spawning, and without a drop in temperature to simulate winter conditions the spawning period was prolonged and release of gametes was not synchronized. Poor synchronization of spawning could result in reduced recruitment, as gametes are wasted and mature specimens die shortly after gamete release.
In Europe, Limecola balthica occurs as far south as the Iberian Peninsula and hence would be expected to tolerate higher temperatures than experienced in Britain and Ireland. Oertzen (1969) recorded that Limecola balthica (as 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 Limecola balthica (as Macoma balthica) from the Humber Estuary, UK, tolerated 6 hours of exposure to temperatures up to 37.5°C with no mortality. Wilson (1981) show that the lethal temperatures for Limecola balthica (as Macoma balthica) change between seasons. Critical temperatures were studied for a Limecola balthica population in Dublin Bay, and a summer maximum of 37.5 and winter maximum of 27.5 were reported (Wilson, 1981). Tolerances were also reported to change with height up the shore, which suggested tolerances adapt to variable conditions.
Despite apparent adaptation to regional temperature ranges, Barda et al. (2014) studied populations of Limecola balthica (as Macoma balthica) in the Baltic Sea and found that increased temperature reduced growth rates. Beukema et al. (2014) also warn that increasing water temperatures as a result of global warming are likely to shorten the growing season (typically late winter to early spring) if warmer spring and summer water temperatures are experienced. Jansen et al. (2007) suggest that temperature increases in the Spanish coast along the Bay of Biscay over the past 40 years caused loss of Limecola balthica populations, due to short-term but frequent exposure to >30° C in the Spanish estuaries, which induced elevated maintenance rates in Limecola balthica, and ultimately starvation. Repeated recruitment failure also occurred after mild winters in a comparable North Sea location, probably due to enhanced survival of predators(Beukema, 1992, Schueckel & Kroencke, 2013; Beukema et al., 2001). As a result, Jansen et al. (2007) predict the southern limit of the species will progressively shift north if temperatures continue to rise.
Pygospio elegans also shows a relationship between timing of reproduction and temperature. Gibson and Harvey (2000) in a study on asexual reproduction of Pygospio elegans in Nova Scotia, Canada found that temperature did not influence reproduction strategy (planktotrophy, lecithotrophy or asexual reproduction) but cite Anger (1984) that environmental conditions, including temperature influence timing of reproduction.
Tubificoides benedii increased in abundance in mudflat habitats in Jade Bay, North Sea between 1930 and 2009 (Schueckel & Kroencke, 2013). Climate warming as well as decreasing nutrient loads and species introductions have occurred in the region since the 1970s, suggesting the species may adapt to temperature increases at benchmark pressures.Bamber & Spencer (1984) observed that Tubificoides were dominant species in an area affected by thermal discharge in the River Medway estuary. Sediments were exposed to the passage of a temperature front of approximately 10oC between heated effluent and estuarine waters during the tidal cycles.
Streblospio shrubsolii have been shown to reproduce in a temperature range of 7.5°C – 30°C with highest reproduction levels occurring between 16°C – 21°C (Levin & Creed, 1986, Dafonsecagenevois & Cazaux, 1987, Chu & Levin, 1989, Lardicci et al., 1997). The evidence was based on Mediterranean sites, limiting confidence for UK and Irish seas. The timing of reproduction and growth, although occurring throughout the year, increased in late spring and early summer but were strongly reduced during periods of higher temperatures in summer and disappeared or were strongly reduced at lower temperatures in winter (Lardicci et al., 1997). The timing of growth and reproduction in Streblospio shrubsolii depended on the synergistic effects of temperature and photoperiod, so that cues may differ at locations at different latitudes (Chu & Levin, 1989). Both a 5°C increase in temp for one month period, or 2°C for one year are within the temperature range reproduction occurs within (7.5°C – 30°C) and within the temperature range where highest reproduction levels occur (16°C – 21°C), suggesting limited impact from the pressure at benchmark pressures is likely.
Higher temperatures have been implicated in the proliferation of trematode parasites which have caused mass mortalities in the snail Hydrobia ulvae (Jensen & Mouritsen, 1992), which is often abundant in this biotope. No other information was found on tolerance of component species to increased temperature. Nevertheless, an increase in temperature may indirectly affect some species as microbial activity within the sediments will be stimulated increasing oxygen consumption and promoting hypoxia.
Sensitivity assessment. Typical surface water temperatures around the UK coast vary, seasonally from 4-19°C (Huthnance, 2010). It is likely that the important characteristic species are able to resist a long-term increase in temperature of 2°C and may resist a short-term increase of 5°C. Limecola balthica may retreat north as a result of long-term warming and climate change. However, the important characterizing species Hediste diversicolor are likely to survive a 5°C increase in temp for one month period, or 2°C for one year, although reproductive activities may be impacted. For instance, without colder winters spawning may not be synchronised and so recruitment would be reduced. A resistance of ‘High’, a resilience of ‘High’ (as longer lived later maturing species are present) and a sensitivity of ‘Not sensitive’ have been assigned.
A decrease in temperature has been shown to be beneficial to Hediste diversicolor as case studies report a reduction in numbers of the species’ predators. For instance, a severe winter in the Wadden Sea in 1995/1996 saw an increased abundance of Hediste diversicolor coincident with a reduction in the numbers of Carcinus maenus and Crangon crangon (Armonies et al., 2001). A similar increase in abundance was noted in the same area between 1978 and 1987 after a series of cold winters (mean Hediste diversicolor density increased from 24/m² to 151/m² respectively ) (Beukema, 1990).
Decreased temperatures throughout the year may limit reproduction. Bartels-Hardege & Zeeck (1990) induced spawning in the laboratory, in specimens of Hediste diversicolor from tidal flats of the Jadebusen (North Sea), outside the normal spawning period of early spring. Temperatures were not lowered to simulate winter conditions but maintained at 16°C. Mature specimens appeared after four weeks and released gametes after a further four weeks according to a semilunar cycle. Reproduction was sustained for a period of four months. Such an extended spawning was witnessed on the Jadebusen following an unusually warm winter. Spawning occurred from February until May and was less synchronized. In contrast, the same population spawned within two months (February - March) following lower winter temperatures in another year. They concluded that not only a threshold temperature was important for synchronized spawning but the timing of the rise in temperature following winter was also a significant factor (Bartels-Hardege & Zeeck, 1990). A reduced rise in temperature is likely to limit this factor.
Colder winter temperatures have been shown to benefit Limecola balthica population dynamics. Recruitment success increased following colder winters and repeated recruitment failure has occurred after mild winters in comparable North Sea location (Beukema, 1992, Schueckel & Kroencke, 2013; Beukema et al., 2001). In Friedrichskoog, Germany, König (1943) found a high accumulation of dead Cerastoderma edule biomass after a severe winter 1936/1937 but high numbers of Limecola balthica (80,000 individuals/m²) spat in following years (winter 1939). Winter water surface temperatures in the Wadden Sea (Netherlands) have increased 1.5°C since the 1980s (Oost et al., 2009). During milder winters greater body weight loss and production of fewer and smaller eggs has been observed in Limecola balthica (van der Meer et al., 2003). It is noted in the literature however, that reduced recruitment success during milder winters may also be due to increased predation as juvenile Crangon crangon have shown increased abundance in relation to milder winters (Beukema & Dekker, 2005).
The geographical distribution of Limecola balthica suggests that it is very tolerant of low temperature. The species occurs in the Gulfs of Finland and Bothnia where the sea freezes for several months of the year (Green, 1968). It must, therefore, resist much lower temperatures than it experiences in Britain and Ireland. Furthermore, Limecola balthica was apparently unaffected by the severe winter of 1962/3, which severely affected many other bivalve species (Crisp, 1964), and De Wilde (1975) noted that Limecola balthica kept at 0°C maintained a high level of feeding activity. It is likely, therefore, that in seas around the UK and Ireland Limecola balthica would be resist decreases in temperature at the pressure benchmark level.
Streblospio shrubsolii has been shown to reproduce in a temperature range of 7.5°C – 30°C with highest reproduction levels occurring between 16°C – 21°C (Levin & Creed, 1986, Da Fonseca-Genevois & Cazaux, 1987, Chu & Levin, 1989, Lardicci et al., 1997). Reproductive activity disappeared or strongly reduced at lower temperatures in winter in a Mediterranean case study (Lardicci et al., 1997), this case study suggests reproduction would be delayed in UK and Irish populations that experienced both a 5°C decrease in temp for one month period, or 2°C for one year.
Sensitivity assessment. The important characterizing species show limited impacts and, potentially, benefits to abundance and recruitment from decreases in temperature. Therefore, a 5°C decrease in temp for one month period, or 2°C for one year is likely to have limited negative impact on all characterizing species in the biotope, within British and Irish seas. Hence, resistance is assessed as ‘High’, resilience is assessed as ‘High’, and sensitivity as ‘Not Sensitive’.
The biotope occurs in variable (18-35 ppt) salinity (JNCC, 2015). The change in salinity assessed as the benchmark is to full salinity (30-35 ppt). The available evidence (summarised below) suggests that the characterizing species are tolerant of an increase to full salinity. The restriction of this biotope to variable salinity is most likely due to the requirement for shelter from wave action rather than salinity regime.
As higher salinity examples of sheltered muddy gravels tend to be more species rich than lower salinity, upper estuarine habitats (Maddock, 2008), it is likely that an increase in salinity at the pressure benchmark will lead to an increase in species richness. An increase at the pressure benchmark may, therefore, lead to the development of the variant sub-biotope LS.LMx.GvMu.HedMx.Scr that occurs in full salinity, or the biotope may survive (where wave action and flows do not increase) but be more species rich.
Hediste diversicolor, the key characterizing species, occurs across all variant sub-biotopes and as such is resistant to the salinity range, from reduced to full, that the various sub-biotopes occur within. Hediste diversicolor is a euryhaline species, able to tolerate a range of salinities from fully marine seawater down to 5 psu or less (Barnes, 1994). Macoma balthica is found in brackish and fully saline waters, although it is more common in brackish waters (Clay, 1967b) so may tolerate variable saliniity. Seitz (2011) found that the distribution of Macoma balthica across a salinity gradient between a minimum and maximum of 8.8psu to 19 psu in Cheaspeake Bay was not influenced by salinity. Instead, resource availability was the principal influence on Macoma balthica. McLusky & Allan (1976) reported that Macoma balthica failed to grow at 41 psu. It is likely that Macoma balthica would be tolerant of an increase in salinity category to fully marine but further increases to >40‰ are likely to affect growth and condition.
Streblospio shrubsolii occurred in subtidal areas of the Thames estuary as well as intertidal flats, suggesting the species is resistant to higher salinities than the ‘variable’ levels occurring higher in estuaries (Attrill, 1998). Likewise Tubificoides benedii has been recorded in high abundance in offshore areas of the North Sea (Gray et al., 1990). Although evidence was limited on response of these species to rapid increases in salinity it is likely they would be resistant to an increase to the fully marine category (30-40 ‰).
Hylleberg (1975) also found that under controlled conditions of salinity ranging from 10 to 30ᵒ⁄ₒₒand temperatures ranging from 5 to 35° C, Hydrobia ulvae has maximal egestion at the combination of high salinity (30ᵒ⁄ₒₒ) and high temperature (30° C). The species would be likely to show high resistance to an increase in salinity from the reduced and variable conditions the biotope occurs within.
Pygospio elegans is common in both marine and brackish waters in the Schelde estuary (Netherlands) suggesting in European habitats the species tolerates a broad salinity range (Ysebaert et al., 1993). Studies of Pygospio elegans population structure in the Baltic Sea and North Sea also found larvae were not hampered by changes in salinity (Kesaniemi et al., 2012). Although case studies are lacking for British and Irish coasts, the existing evidence suggests Pygospio elegans would tolerate salinity changes at the pressure benchmark levels.
Sensitivity assessment. Hediste diversicolor and other characterizing species are likely to tolerate increased salinity levels above the reduced and variable levels encountered in the biotope and variant sub-biotopes. Biotope resistance is, therefore, assessed as ‘High’ and resilience as ‘High’ (by default) and the biotope is considered to be ‘Not sensitive’. In locations with extremely sheltered conditions and gravelly mud is present where the biotope LS.LMx.GvMu.HedMx.Scr characterized by Hediste diversicolor and Scrobicularia plana occurs it is possible a transition to this variant sub-biotope will occur. However, sediment is more likely to be a stronger factor influencing community structure.
The biotope occurs in variable (18-35 ppt) salinity (JNCC, 2015) the decrease in salinity assessed at the benchmark is to low salinity (<18 ppt). The available evidence (summarised below) suggests that the characterizing species are tolerant of a short-term decrease to low salinity but it is likely that for species such as Limecola balthica long-term reductions would lead to mortality.
The key characterizing species Hediste diversicolor is known to tolerate low salinities below 18-24 psu and it has been shown to replace Arenicola marina in areas influenced by freshwater runoff or input (e.g. the head end of estuaries) (Barnes; 1994; Hayward, 1994). Lower salinities (<8 psu) can, however, have an adverse effect on Hediste diversicolor reproduction (Ozoh & Jones, 1990; Smith 1964). Fertilization in Hediste diversicolor is adapted to high salinity but not to low salinity below 7.63‰ (Ozoh & Jones, 1990). A decrease in salinity at the benchmark pressure (reduction to <18‰ ) may negatively impact recruitment and abundance if the dilution is close to that threshold.
Conde et al. (2013) found that Streblospio shrubsolii were a dominant species in low salinity, estuarine conditions (5-9‰) in the Tagus estuary, Portugal. In Ria de Averio, western Portugal Streblospio shrubsolii and Tubificoides benedii were characterizing species of communities in estuarine sample sites further upstream with lower salinity, suggesting a high resistance to a decrease in salinity (Rodrigues et al., 2011).
McLusky & Allan (1976) conducted salinity survival experiments with Limecola balthica (as Macoma balthica) over a period of 150 days. Survival times declined with decreased salinity. At 12 psu specimens survived 78 days, whilst specimens at 8.5 psu survived 40 days. Some specimens of Limecola balthica survived 2.5 days at 0.8 psu, which was apparently due to the animal’s ability to clamp its valves shut in adverse conditions. McLusky & Allan (1976) also reported that Limecola balthica failed to grow (increase shell length) at 15 psu. Limecola balthica is found in brackish and fully saline waters (Clay, 1967b) so may tolerate a state of flux. Its distribution in combination with the experimental evidence of McLusky & Allan (1976) suggests that Limecola balthica is likely to be resistant of decreased salinity over a short period. A decline in salinity in the long-term may have implications for the species viability in terms of growth, and the distribution of the species may alter as specimens at the extremes retreat to more favourable conditions. Metabolic function should, however, quickly return to normal when salinity returns to original levels. Decreased salinity may also affect the ability of Limecola balthica to tolerate contaminants such as heavy metals (see Bryant et al., 1985 & 1985a). Usually, contaminants become more toxic at low salinity (Langston, W.J. pers comm.).
Muus (1967) revealed that Hydrobia ulvae did not crawl into water with a salinity lower than 9ᵒ⁄ₒₒ. Hylleberg (1975) also found that under controlled conditions of salinity ranging from 10 to 30ᵒ⁄ₒₒ and temperatures ranging from 5 to 35°C, shows that Hydrobia ulvae has maximal egestion at the combination of high salinity (30ᵒ⁄ₒₒ) and high temperature (30° C).
Oligochaete dominated biotopes are recorded from a range of salinity regimes from full (LS.LSa.MoSa.Ol; LS.LSa.MoSa.Ol.FS), variable (SS.SMu.SMuVS.CapTubi) reduced (SS.SMu.SMuVS.CapTubi; LS.LMu.UEst.Tben ) and low (SS.SMu.SMuVS.LhofTtub) habitats (JNCC,2015). In very low salinities from <15 to 0 ‰ species such as Limnodrilus spp. and Tubifex tubifex are found (Giere & Pfannkuche, 1982). A decrease in salinity at the pressure benchmark would probably result in replacement by oligochaete species more tolerant of lower salinities such as Limnodrilus hoffmeisteri and Tubifex tubifex that characterize the low salinity biotope SS.SMu.SMuVS.LhofTtub. Numerous studies suggest that Baltidrilus costata tolerates a wide range of salinities from 1‰ to 28‰ (Giere & Pfannkuche, 1982 and references therein), suggesting that this species is likely to still be present in the biotope.
Sensitivity assessment. It is considered likely that a decrease in salinity at the pressure benchmark will lead to some species replacement by polychaetes and oligochaetes more tolerant of low salinity. Hediste diversicolor and oligochaetes are likely to remain but Limecola balthica is likely to reduce in low salinity conditions. A similar biotope could remain where salinities were close to 18 ppt but a severe reduction in salinity would probably lead to loss of the biotope. Resistance is therefore assessed as ‘Low’. Resilience (following restoration of typical conditions) is ‘High’ and sensitivity is assessed as ‘.Low’ It should be noted that resistance would be lower, and sensitivity greater, where salinity was reduced to a level close to freshwater.
Hediste diversicolor characteristically inhabits littoral mudflats predominantly of clay (particles < 4 µm), silt (4-63 µm) and to a lesser extent, very fine sand (63-125 µm) (Jones et al., 2000). Highest abundances occur in very weak (negligible) to weak < 1 knot (<0.5 m/sec.) currents. These conditions are provided by this biotope, which occurs in extremely sheltered gravelly mud to gravelly sandy mud on the mid and lower shore.
The type direction and speed of the currents control sediment deposition within an area. Finer sediment will fall to the substratum in weaker currents. An increase in water flow rate would entrain and maintain particles in suspension and erode the mud. As a result the scouring and consequent redistribution of components of the substratum would alter the extent of suitable habitat available to populations of Hediste diversicolor and other species in the biotope that prefer finer sediment. Recovery of Hediste diversicolor would be influenced by the length of time it would take for the potential habitat to return to a suitable state for recolonization by adult and juvenile specimens from adjacent habitats, and the establishment of a breeding population. Recolonization may take between one and three years, as populations differ in reaching maturity (Dales, 1950; Mettam et al., 1982; Olive & Garwood, 1981), from the time that the habitat again becomes suited to the species.
Coarser sediments are likely to remain in areas of strongest flow velocity (where finer particles have been re-suspended). Species such as Pygospio elegans and other opportunist polychaetes that tolerate coarser particle size will possibly increase in abundance. Limecola balthica is likely to experience greater impact from increased water flow as the species thrives in low energy environments, such as the extremely sheltered areas that characterize the biotope (Tebble, 1976). Increased water flow rate is likely to influence the sediment characteristics in this biotope, primarily by re-suspending and preventing deposition of finer particles (Hiscock, 1983). This is likely to result in erosion of the preferred habitat, which may cause mortality of some portion of the population of Limecola balthica. Higher current velocity (18 cm/s 0.18 m/s) recorded in flume experiments conducted in the Isle of Sylt (North Sea) led to juvenile Limecola balthica being washed out of the sediment (Zuhlke & Reise, 1994). Green (1968) reported that, towards the mouth of an estuary where sediments became coarser and cleaner, Limecola balthica was replaced by another tellin species, Tellina tenuis.
Sensitivity assessment. Limecola balthica abundance may be reduced if juveniles are washed from the substratum. Loss of mud content in some areas is possible and would lead to replacement by another species but this is unlikely at the pressure benchmark levels. An increase in flow velocity may alter sediments, resistance has been assessed as ‘Medium’, recoverability is assessed as ‘High’ and sensitivity is, therefore ‘Low’.
The biotope occurs from the upper to the lower shore (JNCC, 2015) and changes in emergence are unlikely to affect the biotope where it remains within an intertidal habitat. The variant sub-biotopes are found on the lower, mid and upper shopre, with the exception of LS.GvMu.Hedmx.St, which is found on the lower and mid shore (JNCC, 2015).
Hediste diversicolor inhabits a burrow within the sediment which may be up to 0.3 m deep. The species retreats within the burrow during periods of exposure, protecting it from desiccation although increased emergence may cause a decline in the abundance of Hediste diversicolor at the upper limits of the intertidal zone, as they may become stressed by desiccation if the substrata begin to dry and are prone to more extremes of temperature. Hediste diversicolor is sufficiently mobile to gradually retreat back to damper substrata. Gogina et al. (2010) analysed patterns of benthic community distribution related to selected environmental parameters, including depth, in the western Baltic Sea with depths ranging from 0 m to 31 m. Hediste diversicolor displayed a preference for low-saline regions shallower than 18 m. Increased depth had the largest negative effect of all factors influencing distribution and abundance decreased with greater dept) Gogina et al. (2010).
Limecola balthica occurs in the upper regions of the intertidal (Tebble, 1976) and is, therefore, likely to be tolerant of prolonged emergence. It is a bivalve and can close tightly by contraction of the adductor muscle, storing moisture inside the shell. The silty sediments in which the species lives have a high water content and are therefore resistant to desiccation. Furthermore, Limecola balthica is mobile and able to relocate in the intertidal by burrowing (Bonsdorff, 1984) or floating (Sörlin, 1988). It would be expected to react to an increase in emergence by migrating down the shore to its preferred position. There may be an energetic cost to this migration but it is not expected that mortality would result. Limecola balthica should quickly recover from the energetic cost of relocation. Limecola balthica occurs in the intertidal and sublittorally down to depths of 190 m (Olafsson, 1986), although is more abundant intertidally. Hence, it would be expected to resist a decrease in emergence regime. However, a case study, predicting changes in biomass of Limecola balthica in the Humber estuary, UK (western North Sea) under expected sea level rise conditions displayed negative impacts. Coastal squeeze from sea level rise would produce steeper and more homogenous beach face profiles. Limecola balthica was predicted to be lower on steeper beach faces and biomass of Limecola balthica was predicted to decrease (Fujii & Raffaelli, 2008).
Tubificoides benedii is capable of penetrating the substratum to depths of 10 cm, shows a resistance to hypoxia and is often typified as an ‘opportunist’ that is adapted to the rapid environmental fluctuations and harsh conditions in estuaries (Gogina et al., 2010). Highest abundances were predicted by Gogina et al. (2010) to be related to depth with an optimum of 10 m to 20 m. The evidence suggests that abundance may be limited by a decrease in high water level or a change in time (increase) where substratum is not covered by the sea. An increase in the time the biotope is covered by the sea is likely to result in increased abundance of Tubificoides benedii.
Opportunistic, deposit feeding polychaetes, such as Pygospio elegans, Streblospio shrubsolii, Aphelochaeta marioni, Capitella capitata and Manayunkia aestuarina tolerate stressful conditions, and often out-compete more sensitive species in inter-tidal environments due to greater tolerances. Gogina et al. (2010) indicate that Pygospio elegans favours shallower water, but this modelling study suggested the response against increasing depth is not as rapid as in the case of Hediste diversicolor.
Sensitivity assessment. As intertidal species, the biotope and characterizing species are found at a range of shore heights and are considered relatively resistant to changes in emergence which do not alter the extent of the intertidal. An increase in emergence is likely to decrease the upper shore extent of Hediste diversicolor dominated biotopes at the land-ward extent of the intertidal as desiccation increases. A decrease in emergence under the benchmark pressure is likely to extend the upper extent of the biotope as the species recolonize or migrate to favourable conditions. Biotope resistance is, therefore, assessed as ‘High’, recoverability is assessed as ‘High’ (by default) and the biotope is considered to be 'Not sensitive'.
This biotope occurs in wave sheltered areas, where estimated wave categories range from sheltered, very sheltered and extremely sheltered to moderately exposed (JNCC, 2015). The key characterizing species Hediste diversicolor is infaunal, inhabiting a burrow in which it seeks refuge from predators and may partially emerge to seek and capture food. An alteration of factors within the environment that increases wave exposure could cause erosion of the substrata and consequently, loss of habitat.
Wave action stimulates Limecola balthica to start burrowing and individuals have been shown to continue burrowing for a longer period of time than in still water (Breum, 1970). Limited zoobenthic biomass was recorded in areas exposed to strong currents and wave action (Beukema, 2002), limiting food availability, however impacts from this pressure at the benchmark levels may be low for this biotope, as the biotope is limited to sheltered or extremely sheltered locations. Increases in wave action may therefore remain within the limits of the species tolerance but factors such as sediment redistribution may alter the physical biotope. Where less sheltered conditions occur the sub biotope LS.LMx.GvMu.HedMx.Mac is likely to dominate as this variant occurs in the least sheltered conditions.
Sensitivity assessment. Resistance to a change in nearshore significant wave height >3% but <5% of the two main characterizing species Hediste diversicolor and Limecola balthica is ‘High’, given that the biotope occurs across a range of wave exposures and an increase in nearshore significant wave height of >3% but <5% would continue to result in sheltered conditions which are within the species tolerance limits. At the highest benchmark pressure (5% increase) the species exhibit ‘High’ resistance through their traits to live relatively deep in the sediment. Resilience (recoverability) is also ‘High’ giving a Sensitivity of ‘Not Sensitive’. Due to limited evidence, confidence in this assessment is Low.
This pressure is Not assessed but evidence is presented where available. The following review discusses impacts at higher concentrations than the pressure benchmark.
Crompton (1997) reviewed the toxic effect concentrations of metals to marine invertebrates Annelid species, such as Hediste diversicolor were found to be at risk if metals exceeded the following concentrations during 4-14 days of exposure: >0.1 mg Hg l-1, > 0.01 mg Cu l-1, > 1 mg Cd l-1, >1 mg Zn l-1,>0.1 mg Pb l-1, >1 mg Cr L-1, >1 mg As l-1 and >10 mg Ni l-1. In general, for estuarine animals heavy metal toxicity increases as salinity decreases and temperature increases (McLusky et al., 1986). For example, Fernandez & Jones (1990) calculated 96 hour LC50 Zinc values for Hediste diversicolor at four salinities 5, 10, 17.5 and 30 psu at 12°C. The 96 hour LC50 at 17.5 psu and 12°C was 38 mg Zn l-1, while at 5 and 10 psu it was 7 and 19 mg Zn l-1 respectively. Toxicity decreased with increasing salinity. When salinity remained constant at 17.5 psu, but temperature varied, the following 96 hour LC 50 values for Zinc were recorded: 40 mg Zn l-1 at 6°C, 32 mg Zn l-1 at 12°C and 9.1mg Zn l-1 at 20°C. Toxicity increased with increasing temperature. Accumulation of zinc was also greater at the lowest salinities and when the temperature was highest at 20°C. In a parallel experiment, the presence of sediment was found to reduce toxicity and body accumulation of zinc in Hediste diversicolor. Recovery of this species would be influenced by the length of time it would take for the potential habitat to return to a suitable state (e.g. factors such as the decline of bioavailable metals within the marine environment), recolonization by adult and juvenile specimens from adjacent habitats, and the establishment of a breeding population. Since juveniles remain in the infauna throughout their development selection for metal tolerance can be expected to be operative from an early stage (Bryan & Gibbs, 1983).
3) the no-observed-effect concentration (NOEC) for Cu was the lowest dose tested (i.e. 10 µg I-'). (Ruiz et al., 1994).
Alterations of the burrowing behaviour of Scrobicularia plana, were studied in individuals exposed to soluble copper. Animals were exposed for 4 d to concentrations ranging from 25 to 150 μ g Cu l− 1. At the end of exposure, the burrowing kinetics in clean sediment were determined after 1 and 2 days. Even at the lowest tested concentrations, copper caused hypoactivity in organisms belonging to both species studied. Metabolical or physiological disturbances could be the cause of these impairments. Concentrations affecting burrowing behaviour were below those responsible for mortality in these species (Bonnard et al., 2009).
Laboratory tests in clean water can be misleading as these do not reflect lowered toxicity in the marine environment due to the buffering effects of carbon and sulphide which render copper non-labile (not bioavailable) and the influence of water pH, hardness, temperature and salinity etc. Field surveys have found that Scrobicularia plana is present in the highly contaminated Fal Estuary where levels of copper and zinc are high (Bryan & Gibbs, 1983).
Hutchins et al. (1998) described the effect of temperature on bioaccumulation by Limecola balthica of radioactive americium, caesium and cobalt, but made no comment on the intolerance of the species.
Further, direct assessments of impacts at the benchmark pressure on benthic communities, and this biotope in particular were not found.
Sensitivity assessment. No evidence. Insufficient evidence was available to complete and assessment.
The habitats which Hediste diversicolor inhabits tend to have lower oxygen levels than other sediments. Hediste diversicolor is resistant to moderate hypoxia (Diaz & Rosenberg, 1995). Vismann (1990) demonstrated a mortality of only 15% during a 22 day exposure of Hediste diversicolor at 10% oxygen (ca. 2.8 mg O2 per litre). Hediste diversicolor is active at the sediment/water interface where hydrogen sulphide concentrations increase during periods of hypoxia. Vismann (1990) also demonstrated that the high tolerance of Hediste diversicolor to hypoxia in the presence of sulphide is enabled by elevated sulphide oxidation activity in the blood. Hediste diversicolor may also exhibit a behavioural response to hypoxia by leaving the sediment (Vismann, 1990) in the presence of sulphide. After 10 days of hypoxia (10% oxygen saturation) with sulphide (172-187 µmM) only 35% of Hediste diversicolor had left the sediment compared to 100% of Nereis virens. Laboratory experiments in the absence of sediments, found that Hediste diversicolor could survive hypoxia for more than 5 days and that it had a higher tolerance to hypoxia than Nereis virens, Nereis succinea and Nereis pelagica (Theede, 1973; Dries & Theede, 1974; Theede et al., 1973). Juvenile Hediste diversicolor survived hypoxic conditions for 4 days in laboratory conditions and combined hypoxia and increased sulphide (1 mmo1 1-') for 3 days (Gamenick et al., 1996). Post larvae Hediste diversicolor were the only life stage to show les tolerance to hypoxia, surviving for only 14 hr (Gamenick et al., 1996).
Limecola balthica appears to be relatively tolerant of de-oxygenation. Brafield & Newell (1961) frequently observed that, in conditions of oxygen deficiency (e.g. less than 1 mg O2/l), Limecola balthica (as Macoma balthica) displayed survivability of low oxygen concentrations and shell growth continued (Jansson et al., 2015). Although, sub-lethal effects of hypoxia have been identified as individual Limecola balthica moved upwards to fully expose itself on the surface of the sand or buried at shallower depths, leaving them at greater risk of predation (Long et al., 2014). Specimens lay on their side with the foot and siphons retracted but with valves gaping slightly allowing the mantle edge to be brought into full contact with the more oxygenated surface water lying between sand ripples. In addition, Limecola balthica was observed under laboratory conditions to extend its siphons upwards out of the sand in to the overlying water when water was slowly deoxygenated with a stream of nitrogen. The lower the oxygen concentration became the further the siphons extended.
This behaviour, an initial increase in activity stimulated by oxygen deficiency, is of interest because the activity of lamellibranchs is generally inhibited by oxygen deficient conditions (Brafield & Newell, 1961). Dries & Theede (1974) reported the following LT50 values for Limecola balthica (as 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 Limecola balthica to resist extreme oxygen deficiency was mainly due to anaerobic metabolism. Limecola balthica is, therefore very tolerant of hypoxia, although it may react by reducing metabolic activity and predation risk may increase. Metabolic function should quickly return to normal when oxygen levels are resumed and so recovery is expected.
The characterizing oligochaetes and polychaetes within the biotope that display tolerance to hypoxia include Tubificoides benedii and Capitella capitata, while Pygospio elegans is highly sensitive to hypoxia (Gogina et al., 2010). Exposure to dissolved oxygen concentration of less than or equal to 2 mg/l for 1 week is likely to limit Pygospio elegans abundance, whilst having limited impact on Tubificoides benedii and Capitella capitata populations.
This pressure relates to increased levels of nitrogen, phosphorus and silicon in the marine environment compared to background concentrations. The benchmark is set at compliance with WFD criteria for good status, based on nitrogen concentration (UKTAG, 2014). Primary production in the biotope will be limited to microalagae at the sediment surface, rather than macroalgae. Changes in primary production as a result of changes in nutrient enrichment are, therefore, not considered likely to directly alter the biotope.
Aberson et al. (2016) found nutrient enrichment promotes surface deposit feeding in Hediste diversicolor, over suspension feeding and predation. At sewage-polluted sites in three estuaries in SE England Hediste diversicolor mainly consumed microphytobenthos, sediment organic matter and filamentous macroalgae Ulva spp. At cleaner sites Hediste diversicolor relied more on suspension feeding and consumption of Spartina anglica (Aberson et al., 2016). Whilst suggesting adaptability to nutrient enrichment this behaviour will increase predation risk.
Nutrient enrichment favours the growth of opportunistic green macro-algae blooms which can cause declines in some species and increases in others (Raffaelli, 2000). Evidence (Beukema, 1989; Reise et al., 1989; Jensen, 1992) suggested a doubling in the abundance of Hediste diversicolor in the Dutch Wadden Sea, accompanied by a more frequent occurrence of algal blooms that were attributed to marine eutrophication. Algae may be utilized by Hediste diversicolor in its omnivorous diet, so some effects of nutrient enrichment may be beneficial to this species. However, evidence for the effects of algal blooms stimulated by nutrient enrichment on Hediste diversicolor is not consistent. Raffaelli (1999) examined a 30 year data base to examine the effect of nutrient enrichment on an estuarine food web in Aberdeenshire, Scotland. This study displayed impacts to species characterizing the biotope from development of algal mats, the density and distribution of which was related to nutrient. In areas where algal biomass was greatest reduced invertebrate densities were recorded. The mud shrimp Corophium volutator showed the greatest decrease in density. Densities of Corophium volutator, Limecola balthica and Hediste diversicolor were lower in 1990 compared to 1964 at sites where macro-algal mats increased over the same period. Conversely, densities were on average higher in the upper reaches where macroalgal mats were generally absent before 1990 (Raffaelli, 1999). Capitella capitata and Pygospio elegans abundance were greater in areas that received greatest nutrient enrichment (Raffaelli, 1999). Long-term nutrient enrichment may, therefore, alter the biotope if high biomass of algal mats persists.
Sensitivity assessment. The benchmark is relatively protective and is not set at a level that would allow blooms of green algae on the sediment, based on this consideration and based on the lack of primary producers structuring the biotope, resistance is assessed as 'High' and resilience as 'High' (by default), so that the biotope is assessed as 'Not sensitive'.
All species apart from two that are abundant in the biotope are classed in a Marine Biotic Index as being indifferent to, tolerating or proliferating under organic enrichment conditions (Borja et al., 2000). Only Limecola balthica and Manayunkia aestuarina are recorded as being sensitive to organic enrichment.
However, case studies display resilience of Limecola balthica populations to enrichment. Limecola balthica (as Limecola balthica) has been shown experimentally to be able to resist periods of up to nine weeks under algal clover, their long siphon allowing them to reach oxygenated water although other bivalves decreased in abundance (Thiel et al., 1998). Organic enrichment from waste-water discharge in the Dutch Wadden Sea resulted in positive effects on Limecola balthica abundance, biomass, shell growth and production. These effects were concluded to be due to increased food supply (Madsen & Jensen, 1987). Tubificoides benedii and other oligochaetes are very tolerant of high levels of organic enrichment and often dominate sediments where sewage has been discharged or other forms of organic enrichment have occurred (Pearson & Rosenberg, 1978; Gray, 1971; McLusky et al., 1980).
Sensitivity assessment. At the benchmark levels, a resistance of ‘High’ as the main characterizing species Hediste diversicolor is tolerant of organic enrichment and an input at the pressure benchmark is considered unlikely to lead to gross pollution effects . A resilience of ‘High’ is assigned (by default) and the biotope is assessed as ‘Not sensitive’.
This biotope and sub-biotopes is only found in sediment, in particular, gravelly sandy mud or gravelly mud (JNCC, 2015). The burrowing organisms characterizing this biotope, including Hediste diversicolor, and Limecola balthica would not be able to survive if the substratum type was changed to either a soft rock or hard artificial type. Consequently, the biotope would be lost altogether if such a change occurred.
Sensitivity assessment. Biotope resistance is assessed as ‘None’, resilience is ‘Very low’ (as the change at the pressure benchmark is permanent) and biotope sensitivity is ‘High’.
The benchmark for this pressure refers to a change in one Folk class. The pressure benchmark originally developed by Tillin et al. (2010) used the modified Folk triangle developed by Long (2006) which simplified sediment types into four categories: mud and sandy mud, sand and muddy sand, mixed sediments and coarse sediments. The change referred to is, therefore, a change in sediment classification rather than a change in the finer-scale original Folk categories (Folk, 1954). The biotope occurs in mud or sandy mud (JNCC, 2015). At the pressure benchmark a change in sediment to increased coarse sediment content (to gravels or sands) is considered. An increase in gravel and a change to clean sands or coarse sediments is likely to have a more significant effect as sediment cohesion and ability to retain organic matter and water is reduced altering habitat suitability for burrowing polychaetes and amphipods and deposit feeders.
Hediste diversicolor is infaunal and is reliant upon a muddy/sandy sediment in which to burrow. Hediste diversicolor has been identified in other intertidal sediments including gravels, clays and even turf (Clay, 1967; Scaps, 2002), although abundance may be reduced in these habitats. Limecola balthica is likely to tolerate increased gravel content as sediment was not shown to affect burrowing (Tallqvist, 2001), however, growth, shell size and body mass were greatest in higher sand content sediment and lower in higher gravel content sediments (Azouzi et al. 2002), suggesting long-term health and abundance may be affected by a permanent increase in gravel content. Conde et al. (2011) compared recruitment of Scrobicularia plana to excavated and un-excavated control plots (expected to enhance the deposition of bivalve spat if the settlement of bivalves was the result of a passive process) at different shore levels in Portugal. Juveniles were found to avoid excavated plots, showing significantly higher abundance in control plots. The data strongly suggested that recruited bivalves actively avoid unsuitable substrata, including an increased gravel fraction.
Coarser sediments provide inhospitable conditions for colonizing infauna, although Pygospio elegans show greater tolerance of increased gravel content and are viewed as opportunistic species that are capable of exploiting these inhospitable conditions (Gray, 1981). Therefore, Pygospio elegans are likely to be less affected and even increase in abundance under a change in Folk class to gravelly mud (or a change from sandy mud to muddy sand, or gravelly muddy sand). Capitella capitata are likely to decrease in abundance as Degraer et al. (2006) found that Capitella capitata in the Belgium part of the North Sea were almost completely absent in sediments without mud. Similar species that prefer higher organic content may also show limited abundance in more gravelly sediments.
Sensitivity assessment. Case studies display decreasing abundance with increased gravel content (Hediste diversicolor) and reduced growth rates (Limecola balthica). Abundance of abundant polychaetes is likely to depend on each species tolerance of increasing gravel content, with species that can exploit the conditions increasing in abundance (Pygospio elegans) but other species decreasing in abundance. Resistance to a change in one Folk class is assessed as ‘Low’ as biotopes are likely to change to corresponding muddy sediment biotope or increased gravel content is likely to lead to reduced abundance of characterizing species. Resilience is assessed as ‘Very Low’ as a change at the benchmark is permanent. The sensitivity of the biotope overall is, therefore, considered to be ‘High’.
The substratum of this biotope consists of sandy mud or mud (JNCC, 2015). The characterizing infaunal species, including Hediste diversicolor and Limecola balthica burrow into the sediment, to depths not exceeding 30 cm. The process of extraction is considered to remove all biological components of the biotope group in the impact footprint and the sediment habitat.
Sensitivity assessment. Resistance to extraction of substratum to 30 cm across the entire biotope is assessed as ‘None’ based on expert judgment but supported by the literature relating to the position of these species on or within the seabed and literature on impacts of dredging and bait digging activities (see penetration and disturbance pressure). At the pressure benchmark the exposed sediments are considered to be suitable for recolonization almost immediately following extraction. Recovery will be mediated by the scale of the disturbance and the suitability of the sedimentary habitat, biotope resilience is assessed as 'High' (based on recolonization by adults and pelagic larvae) and biotope sensitivity is assessed as 'Medium'.
Mud and sandy mud sediments, in general, tend to be cohesive although high levels of water content will reduce this and destabilise sediments. Sediment cohesion provides some sediment stabilisation to resist erosion following surface disturbance. The characterizing species associated with this biotope are infaunal and hence have some protection against surface disturbance, although siphons of bivalves and tubes of the sedentary polychaete Pygospio elegans, may project above the sediment surface. Damage to tubes and siphons would require repair. The snail Hydroia ulvae is present on the surface and abrasion may result in burial or damage to this species. Surface compaction can collapse burrows and reduce the pore space between particles, decreasing penetrability and reducing stability and oxygen content (Sheehan, 2007). Trampling (3 times a week for 1 month) associated with bait digging reduced the abundance and diversity of infauna (Sheehan, 2007; intertidal muds and sands). The bivalve Scrobicularia plana has a hard shell and can retreat into a long, protective tube, providing some protection from abrasion. Trampling experiments used to assess the impacts of crab-tiling have shown an increase in Scrobicularia plana in trampled plots, indicating that this species has some resistance to this pressure (Sheehan et al., 2010).
Sensitivity assessment. Resistance is assessed as ‘Medium', as abrasion is unlikely to affect high numbers of infaunal burrowing species such as the key characterizing species Hediste diversicolor and the oligochaetes but bivalves, tube dwelling polychaetes and Hydrobia ulvae, may be reduced in abundance. Resilience is assessed as 'High' and biotope sensitivity is assessed as 'Low'.
As the characterizing species are burrowing species, the impact from damage to the sub-surface sea bed would be greater than damage to the sea bed surface only (see abrasion pressure). A number of studies have assessed the impacts of activities resulting in penetration and disturbance of sediments on the characterizing species in similar habitats. The characterizing species have some protective traits such as infaunal life habit, with deeper burrowing species less exposed. The shells of Scrobicularia plana and Limecola balthica provide some protection. Pygospio elegans inhabits fragile tubes at the sediment surface and Hydrobia ulvae crawl on the sediment, both species are likely to be vulnerable to penetration and disturbance of the sediment. Ferns et al. (2000) studied effects of harvesting of cockles and reported a decline in muddy sands of 83% in Pygospio elegans (initial density 1850 m−2) when a mechanical tractor towed harvester was used in a cockle fishery. Pygospio elegans and Hydrobia ulvae were significantly depleted for >100 days after harvesting (surpassing the study monitoring timeline).
Rees, 1978, (cited in Hiscock et al., 2002), assessed pipe laying activities. The pipe was laid in a trench dug by excavators and the spoil from the trenching was then used to bury the pipe. The trenching severely disturbed a narrow zone, but a zone some 50 m wide on each side of the pipeline was also disturbed by the passage of vehicles. The tracked vehicles damaged and exposed shallow-burrowing species such as the bivalves Cerastoderma edule and Limecola balthica, which were then preyed upon by birds. Deeper-dwelling species were apparently less affected; feeding-marks made by the bivalve Scrobicularia plana were both observed in the vehicle tracks. During the construction period, the disturbed zone was continually re-populated by mobile organisms, such as Hydrobia ulvae.
The effects of a pipeline construction on benthic invertebrates were also investigated using a Before/After impact protocol at Clonakilty Bay, West Cork, Ireland. Benthic invertebrates were sampled once before the excavation and at one, two, three and six months after the completion of the work. Invertebrate samples were dominated by Hediste diversicolor, Scrobicularia plana and Tubifex spp. An impact was obvious in the construction site in that no live invertebrates were found at one month after disturbance, but there followed a gradual recolonisation by Hediste diversicolor. At six months after the disturbance there was no significant difference in the mean number of total individuals (of all species) per core sample amongst all study sites, but the apparent recovery in the impacted area was due to two taxa only, Hediste diversicolor and Tubifex spp. (Lewis et al., 2002).
Sensitivity assessment. Resistance of the biotope is assessed as ‘Low’, although the significance of the impact for the bed will depend on the spatial scale of the pressure footprint. Resilience is assessed as ‘High’, and sensitivity is assessed as ‘Low’.
Changes in light penetration or attenuation associated with this pressure are not relevant to Hediste diversicolor and Limecola balthica biotopes. As the species live in the sediment they are also likely to be adapted to increased suspended sediment (and turbidity). However, alterations in the availability of food or the energetic costs in obtaining food or changes in scour could either increase or decrease habitat suitability for Hediste diversicolor, Limecola balthica as characterizing species and for other abundant species such as the oligochaetes Tubificoides benedii and Tubificoides pseudogaster.
Hediste diversicolor characteristically inhabits estuaries where turbidity is typically higher than other coastal waters. Changes in the turbidity may influence the abundance of phytoplankton available as a food source that may be attained through filter feeding. Hediste diversicolor utilizes various other feeding mechanisms and, at the benchmark level, the likely effects of a change in one rank on the WFD scale are limited.
Scrobicularia plana does not require light and therefore would not be affected by a decrease in turbidity for light attenuation purposes. It is possible that decreased turbidity would increase primary production in the water column and by micro-phyto benthos. The resultant increase in food availability may enhance growth and reproduction in this species, but only if food was previously limiting.
Sensitivity assessment. The following sensitivity assessment relies on expert judgement, utilising evidence of species traits and distribution and therefore confidence has been assessed as low. Resistance is ‘High’ as no significant negative effects are identified and potential benefits from increased food resources may occur. Resilience is also ‘High’ as no recovery is required under the likely impacts. Sensitivity of the biotope is, therefore, assessed as ‘Not Sensitive’.
The degree to which the characterizing species are able to resist this pressure depends primarily on species mobility, ability to survive within sediment without contact with the surface and ability to escape from the over-burden. Factors that affect the ability to regain the surface include grain size (Maurer et al., 1986), temperature and water content (Chandrasekara & Frid, 1998).
Mobile polychaetes have been demonstrated to burrow through thick layers of deposits. Powilleit et al., (2009) studied the response of the polychaete Nephtys hombergii to smothering. This species successfully migrated to the surface of 32-41 cm deposited sediment layer of till or sand/till mixture and restored contact with the overlying water. While crawling upward to the new sediment surfaces burrowing velocities of up to 20 cm/day were recorded for Nephtys hombergii. Similarly, Bijkerk (1988, results cited from Essink 1999) indicated that the maximal overburden through which species could migrate was 60 cm through mud for Nephtys and 90 cm through sand. No further information was available on the rates of survivorship or the time taken to reach the surface.
Tubificoides spp. and other oligochaetes live relatively deeply buried and can tolerate periods of low oxygen that may occur following the deposition of a fine layer of sediment. Tubificoides spp. showed some recovery through vertical migration following the placement of a sediment overburden 6cm thick on top of sediments (Bolam, 2011). Whomersley et al., (2010) experimentally buried plots on intertidal mudflats at two sites (Creeksea- Crouch Estuary, England and Blackness- lower Forth Estuary, Scotland), where Tubificoides benedii were dominant species. For each treatment anoxic mud was spread evenly to a depth of 4 cm on top of each treatment plot. The mud was taken from areas adjacent to the plots, and was obtained by scraping off the surface oxic layer and digging up the underlying mud from approximately 20 cm depth. Plots were subject to either low intensity treatments (burial every four weeks) or high (burial every two weeks). The experiment was carried out for 10 months at Creeksea and a year at Blackness. At Creeksea numbers of Tubificoides benedii increased in both burial treatments until the third month (high burial) and sixth month (low burial). At Blackness increased numbers ofTubificoides benedii were found in both burial treatments after one month (Whomersley et al., 2010).
Laboratory experiments have shown that the snail Hydrobia ulvae can rapidly resurface through 5cm thick fine deposits, although this ability is reduced where deposited sediments contain little water (Chandrasekara & Frid, 1998). Field experiments where 10 cm of sediment were placed on intertidal sediments to investigate the effects of the beneficial use of dredged materials found that the abundance of Hydrobia ulvae had returned to ambient levels within 1 week (Bolam et al., 2004).
Limecola balthica is able to burrow both vertically and horizontally through the substratum. It is likely that Limecola balthica is not sensitive to smothering by a layer of sediment 5 cm thick as it is a mobile species able to burrow upwards and surface from a depth of 5 - 6 cm (Brafield & Newell, 1961; Brafield, 1963; Stekoll et al., 1980). Turk and Risk (1981) investigated the effect of experimentally induced sedimentation (through fences and boxes that induced sediment deposition on intertidal mudflats in the Bay of Fundy), of 1-3.5cm at a rate of 1.9-10.2 cm/month. The results showed that Limecola balthica was generally unaffected.
The associated species Pygospio elegans is limited by high sedimentation rates (Nugues et al., 1996) and the species does not appear to be well adapted to oyster culture areas where there are high rates of accumulation of faeces and pseudo faeces (Sornin et al., 1983; Deslous-Paoli et al., 1992; Mitchell, 2006 and Bouchet & Sauriau 2008). Pygospio elegans is known to decline in areas following re-deposition of very fine particulate matter (Rhoads & Young, 1971; Brenchley, 1981). Experimental relaying of mussels on intertidal fine sands led to the absence of Pygospio elegans compared to adjacent control plots. The increase in fine sediment fraction from increased sediment deposition and biodeposition alongside possible organic enrichment and decline in sediment oxygen levels was thought to account for this (Ragnarsson & Rafaelli, 1999).
The amphipod Corophium volutator may be sensitive to deposits at the pressure benchmark. Experimental fences placed on mudflats that caused sedimentation rates of 2-2.5 cm/month and reduced Corophium volutator densities from approximately 1700 m² to approximately 400 m². In areas without fences,Corophium volutator numbers increased from approximately 1700 per m² to 3500 per m² (Turk & Risk, 1981).
In intertidal mudflats with similar characterizing species, experiments testing the effects of deposition of sediments typical of beach recharge, have found that recovery of biological assemblages is complete within two years (Bolam & Whomersley, 2003).
Sensitivity assessment. As the exposure to the pressure is for a single discrete event, resistance is assessed as ‘Medium’ as some species associated with the biotope such as Corophium volutator and Pygospio elegans may decline but the biotope is likely to be recognizable within a week due to repositoing and migration of mobile species. Resilience is assessed as ‘High’ and sensitivity is assessed as ‘Low.
Studies have found that beach ‘replenishment’ or ‘nourishment’ that involves the addition of sediments on beaches can have a number of impacts on the infauna (Peterson et al., 2000; Peterson et al., 2006). Impacts are more severe when the sediment added differs significantly in grain size or organic content from the natural habitat (Peterson et al., 2000).
Hediste diversicolor inhabits depositional environments. It is capable of burrowing to depths of up to 0.3 m and reworking sub-surface modifications of its burrow through fine clays and sand. Smith (1955) found no appreciable difference in the population of a Hediste diversicolor colony which had been covered by several inches of sand through which the worms tunnelled. Mobile polychaetes have been demonstrated to burrow through thick layers of deposits. Powilleit et al., (2009) studied the response of the polychaete Nephtys hombergii to smothering. This species successfully migrated to the surface of 32-41 cm deposited sediment layer of till or sand/till mixture and restored contact with the overlying water. While crawling upward to the new sediment surfaces burrowing velocities of up to 20 cm/day were recorded for Nephtys hombergii. Similarly, Bijkerk (1988, results cited from Essink 1999) indicated that the maximal overburden through which species could migrate was 60 cm through mud for Nephtys and 90 cm through sand. No further information was available on the rates of survivorship or the time taken to reach the surface.
Witt et al. (2004) identified an increase in Limecola balthica (as Macoma balthica) abundance in areas of disposal of dredge waste spoil, possibly due to nutrient input at the disposal site. This suggests Limecola balthica responds opportunistically to this pressure.
In intertidal mudflats with similar characterizing species, experiments testing the effects of deposition of sediments, typical of beach recharge have found that recovery of biological assemblages is complete within two years (Bolam & Whomersley, 2003).
Sensitivity assessment. Deposition of up to 30 cm of fine material is likely to provide different impacts for the different species characterizing the biotope. Overall, although the characterizing species have some resistance to this to this pressure, but populations are likely to be reduced. Resistance to initial smothering is ‘Low’ Resilience is ‘High’ and biotope sensitivity is assessed as ‘Low’.
Examples of the impact of specific marine litter, including cigarette butts and micro-plastics are also considered..
Litter, in the form of cigarette butts has been shown to have an impact on ragworms. Hediste diversicolor showed increased burrowing times, 30% weight loss and a >2 fold increase in DNA damage when exposed to water with toxicants (present in cigarette butts) in quantities 60 fold lower than reported from urban run-off (Wright et al., 2015). This UK study suggests health of infauna populations are negatively impacted by this pressure.
Studies of other characterizing species in relation to micro plastics were not available. However, studies of sediment dwelling, sub surface deposit feeding worms, showed negative impacts from ingestion of micro plastics. For instance, Arenicola marina ingests micro-plastics that are present within the sediment it feeds within. Wright et al. (2013) carried out a lab study that displayed presence of micro-plastics (5% UPVC) significantly reduced feeding activity when compared to concentrations of 1% UPVC and controls. As a result, Arenicola marina showed significantly decreased energy reserves (by 50%), took longer to digest food, and as a result decreased bioturbation levels which would be likely to impact colonisation of sediment by other species, reducing diversity in the biotopes the species occurs within. Wright et al. (2013) also present a case study based on their results, that in the intertidal regions of the Wadden Sea, where Arenicola marina is an important ecosystem engineer, Arenicola marina could ingest 33 m² of micro-plastics a year.
Sensitivity assessment. Marine litter in the form of cigarette butts or micro plastics health of populations of characterizing species may be impacted. Significant impacts have been shown in laboratory studies but impacts at biotope scales are still unknown. Evidence and confidence in the assessment is limited and this pressure is 'Not assessed'.
There is no evidence on effects of electric and magnetic fields on the characterizing species.
Electric and magnetic fields generated by sources such as marine renewable energy device/array cables may alter behaviour of predators and affect infauna populations. Evidence is limited and occurs for electric and magnetic fields below the benchmark levels, confidence in evidence of these effects is very low.
Field measurements of electric fields at North Hoyle wind farm, North Wales recorded 110µ V/m (Gill et al., 2009). Modelled results of magnetic fields from typical subsea electrical cables, such as those used in the renewable energy industry produced magnetic fields of between 7.85 and 20 µT (Gill et al. 2009; Normandeau et al. 2012). Electric and magnetic fields smaller than those recorded by in field measurements or modelled results were shown to create increased movement in potential predators of Hediste diversicolor, thornback ray Raja clavata and attraction to the source in catshark Scyliorhinus canicular (Gill et al. 2009).
Flatfish species which are predators of many polychaete species including dab Limanda limanda and sole Solea solea have been shown to decrease in abundance in a wind farm array or remain at distance from wind farm towers (Vandendriessche et al., 2015; Winter et al. 2010). However, larger plaice increased in abundance (Vandendriessche et al., 2015). There have been no direct causal links identified to explain these results.
Species within the biotope can probably detect vibrations caused by noise and in response may retreat in to the sediment for protection. However, at the benchmark level the community is unlikely to be sensitive to noise and this therefore is ‘Not relevant’.
There is no direct evidence of effects of changes in incident light on the characterizing species of this biotope. All characterizing species live in the sediment and do not rely on light levels directly to feed or find prey so limited direct impact is expected. As this biotope is not characterized by the presence of primary producers, shading is unlikely to alter the character of the habitat directly and this pressure is considered 'Not relevant'.
More general changes to the productivity of the biotope may, however, occur. Beneath shading structures there may be changes in microphytobenthos abundance. Littoral mud and sand support microphytobenthos on the sediment surface and within the sediment. Mucilaginous secretions produced by these algae may stabilise fine substrata (Tait & Dipper, 1998).
Shading will prevent photosynthesis leading to death or migration of sediment microalgae altering sediment cohesion and food supply to higher trophic levels. The impact of these indirect effects is difficult to quantify.
Barriers that reduce the degree of tidal excursion may alter larval supply to suitable habitats from source populations. Barriers may also act as stepping stones for larval supply over greater distances (Adams et al., 2014).
Conversely, the presence of barriers at brackish waters may enhance local population supply by preventing the loss of larvae from enclosed habitats to environments, which are unfavourable, reducing settlement outside of the population.
If a barrier (such as a tidal barrier) incorporated renewable energy devices such as tidal energy turbines, these devices may affect hydrodynamics and so migration pathways for larvae into and out of the biotope (Adams et al., 2014). Evidence on this pressure is limited.
Capitella capitata and the associated species Pygospio elegans are capable of both benthic and pelagic dispersal. In the sheltered waters where this biotope occurs, with reduced water exchange, in-situ reproduction may maintain populations rather than long-range pelagic dispersal. As the tubificid oligochaetes that characterize this biotope have benthic dispersal strategies (via egg cocoons laid on the surface (Giere & Pfannkuche, 1982), water transport is not a key method of dispersal over wide distances.
Sensitivity assessment. Resistance to this pressure is assessed as 'High' and resilience as 'High' by default. This biotope is therefore considered to be 'Not sensitive'.
Characterizing species and have limited, visual perception, this pressure is therefore considered 'Not relevant'.
Important characterizing species within this biotope are not cultivated or translocated. This pressure is therefore considered ‘Not relevant’ to this biotope group.
Intertidal sediments may be colonized by a number of invasive non-indigenous species. Invasive species that alter the character of the biotope or that predate on characterizing species are most likely to result in significant impacts. Intertidal flats may be colonized by the invasive non-indigenous species Crepidula fornicata and the pacific oyster Magallana gigas. The two species have not only attained considerable biomasses from Scandinavian to Mediterranean countries but have also generated ecological consequences such as alterations of benthic habitats and communities and food chain changes (OSPAR, 2009b).
In the Wadden Sea, the Pacific oyster Magallana gigas has colonized intertidal flats (Smaal et al., 2005). This species consumes pelagic larvae reducing recruitment (Smaal et al., 2005). The most severe effects are likely to occur from impacts on sediment, where Magallana gigas create reefs on sedimentary flats that will prevent recruitment of juveniles and will restrict access of infauna to the sediment-water interface impacting respiration and feeding of bivalves such as Limecola balthica and Scrobicularia plana and polychaetes such as Pygospio elegans and disturbing the amphipod Corophium volutator. Burrowing infauna such as Hediste diversicolor and oligochaetes may persist within sediments but the overall character of the mixed sediment biotope would be altered.
The Manila clam (Tapes philippinarium), which was introduced to Poole Harbour for aquaculture in 1998, has become a naturalised population on the intertidal mudflats (occurring at densities of 60 clams/m2 in some locations within the harbour (Jensen et al. 2004, cited in Caldow et al. 2007). Densities of Cerastoderma edule and Abra tenuis increased following the introduction of the Manila clam although the abundance of Scrobicularia plana and Limecola balthica declined (Caldow et al., 2005), although the decline of these species may have been caused by tri-butyl tin pollution (Langston et al., 2003) and may have facilitated the naturalization of the Manila clam.
The predatory veined whelk (Rapana venosa) and Hemigrapsus takinei are not established in the UK (although Hemigrapsus takinei has been recorded at two locations) could become significant predators of Cerastoderma edule and other species associated with the biotope in the future.
Sensitivity assessment. Intertidal muddy sands may be exposed to invasive species which can alter the character of the habitat (primarily Crepidula fornicata at the sublittoral fringe and Magallana gigas) leading to re-classification of this biotope, the biotope is considered to have ‘Low’ resistance and ‘Very low’ recovery (unless invasive species are removed). Biotope sensitivity is, therefore, assessed as ‘High’.
Limited evidence was returned by searches on the effect on Hediste diversicolor of introduction of relevant microbial pathogens or metazoan disease vectors to an area where they are currently not present. Desrina et al. (2014) failed to induce infection of the ‘White Spot Shrimp’ virus that can cause large scale mortality in shrimp in Hediste diversicolor by both feeding and immersion.
Sensitivity assessment. Evidence and so confidence is limited, resistance is assessed as ‘High’, resilience is assessed as ‘High’ and sensitivity is, therefore assessed as ‘Not sensitive’.
The sedimentary biotope and characterizing and associated species may be disturbed and damaged by static or mobile gears that are targeting other species. These direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures. The sensitivity assessment for this pressure considers any biological/ecological effects resulting from the removal of target species on this biotope. Ragworms Hediste diversicolor are targeted by recreational and commercial bait diggers. The extent of the impact will depend on the fishing / removal method and spatial extent.
Populations of Hediste diversicolor are dominated by females; males may constitute up to 40% of the population but several reports suggest that the proportion of males is frequently lower (< 20%) (see Clay, 1967c). The sexes are externally indistinguishable except when approaching maturation and during spawning (see reproduction and adult general biology).
Consequently extraction e.g. by bait digging, of 50% of the specimens from within an area is likely to remove more females than males. A reduction in the female proportion of the population prior to spawning could reduce recruitment to the population. The mechanical action of the digging, even if the worms were not actually taken, may also cause some damage to the bodies. Recovery is dependent on the reproductive success and survival of the remaining population and colonization by adults from unaffected areas.
Sensitivity assessment. The key, characterizing species Hediste diversicolor may be targeted and their removal will alter the character of the biotope. Due to potential impacts on Hediste diversicolor populations, in particular females, biotope resistance is assessed as ‘Low’. Biotope resilience is assessed as ‘High’ biotope sensitivity is assessed as ‘Low’.
Direct, physical impacts are assessed through the abrasion and penetration of the seabed pressures, while this pressure considers the ecological or biological effects of by-catch. Species in these biotopes, including the characterizing species, may be damaged or directly removed by static or mobile gears that are targeting other species (see abrasion and penetration pressures). Loss of these species would alter the character of the biotope resulting in re-classification, and would alter the physical structure of the habitat resulting in the loss of the ecosystem functions such as secondary production performed by these species.
Sensitivity assessment. Removal of the characterizing species would result in the biotope being lost or reclassified. Thus, the biotope is considered to have a resistance of Low to this pressure and to have High resilience, resulting in the sensitivity being judged as Low.
Caddy, J.F., 1967. Maturation of gametes and spawning in Macoma balthica (L.). Canadian Journal of Zoology, 45, 955-965.
Caldow, R., McGrorty, S.,West, A., Durell, S. E. A. le V. dit, Stillman, R.,Anderson, S. 2005. Macro-invertebrate fauna in the intertidal mudflats. In The ecology of Poole Harbour (eds J. Humphreys & V. May), pp. 91–108. Amsterdam, The Netherlands: Elsevier B.V.
Caldow, R.W.G., Stillman, R.A., le V. dit Durell, S.E.A., West, A.D., McGrorty, S., Goss-Custard, J.D., Wood, P.J. & Humphreys, J., 2007. Benefits to shorebirds from invasion of a non-native shellfish. Proceedings of the Royal Society, B. 274, 1449 – 1455.
Chu, J.W. & Levin, L.A., 1989. Chu, J.W. & Levin, L.A., 1989. Photoperiod and temperature regulation of growth and reproduction in Streblospio benedicti (Polychaeta: Spionidae). Invertebrate Reproduction & Development, 15 (2), 131-142.
Clay, E., 1967b. Literature survey of the common fauna of estuaries, 10. Macoma balthica and Tellina tenuis. Imperial Chemical Industries Limited, Brixham Laboratory, BL/A/705.
Conde, A., Novais, J.M. & Domínguez, J., 2011. A field experiment on the reproductive success of the invasive clam Mya arenaria (Bivalvia) in the Tagus estuary: coexistence with the native clam Scrobicularia plana. Scientia Marina, 75, 301-308.
Conde, A., Novais, J.M. & Domínguez, J., 2013. Characterization of an estuarine environment by means of an index based on intertidal macrofauna. Marine Pollution Bulletin, 71 (1–2), 129-138.
Crompton T.R., 1997. Toxicants in the aqueous ecosystem. New York: John Wiley & Sons.
Da Fonseca-Genevois, V. & Cazaux, C., 1987. Streblospio benedicti Webster, 1879 (Annelida, Polychaeta) in the Loire Estuary - biology and ecology. Cahiers de Biologie Marine, 28 (2), 231-261.
De Wilde, P.A.W., 1975. Influence of temperature on behaviour, energy metabolism and growth of Macoma balthica (L.). In Barnes, e.H. In Ninth European Marine Biology Symposium Aberdeen University Press, pp. 239-256.
Degraer, S., Wittoeck, J., Appeltans, W., Cooreman, K., Deprez, T., Hillewaert, H., Hostens, K., Mees, J., Berge, V. & Vincx, M., 2006. The macrobenthos atlas of the Belgian part of the North Sea. Belgian Science Policy.
Deslous-Paoli, J.-M., Lannou, A.-M., Geairon, P., Bougrier, S., Raillard, O. & Héral, M., 1992. Effects of the feeding behavior of Crassostrea gigas (Bivalve Molluscs) on biosedimentation of natural particulate matter. Hydrobiologia, 231 (2), 85-91.
Desrina, Verreth, J.A.J., Vlak, J.M. & Verdegem, M.C.J., 2014. Hediste diversicolor (O.F. Mueller 1776) as a Possible Model to Study White Spot Syndrome Virus Infection in Polychaetes. Asian Fisheries Science, 27 (3), 199-211.
Dittmann, S., Günther, C-P. & Schleier, U., 1999. Recolonization of tidal flats after disturbance. In The Wadden Sea ecosystem: stability, properties and mechanisms (ed. S. Dittmann), pp.175-192. Berlin: Springer-Verlag.
Emerson, C.W. & Grant, J., 1991. The control of soft-shell clam (Mya arenaria) recruitment on intertidal sandflats by bedload sediment transport. Limnology and Oceanography, 36, 1288-1300.
Fujii, T. & Raffaelli, D., 2008. Sea-level rise, expected environmental changes, and responses of intertidal benthic macrofauna in the Humber estuary, UK. Marine Ecology Progress Series, 371, 23-35.
Gilbert, M.A., 1978. Aspects of the reproductive cycle in Macoma balthica (Bivalvia). The Nautilus, 29, 21-24.
Green, J., 1968. The biology of estuarine animals. Sidgwick and Jackson, London.
Grilo, T.F., Cardoso, P.G., Dolbeth, M., Bordalo, M.D. & Pardal, M.A., 2011. Effects of extreme climate events on the macrobenthic communities' structure and functioning of a temperate estuary. Marine Pollution Bulletin, 62 (2), 303-311.
Guenther, C.P., 1991. Settlement of Macoma balthica on an intertidal sandflat in the Wadden Sea. Marine Ecology Progress Series, 76, 73-79.
Harvey, M. & Vincent, B., 1989. Spatial and temporal variations of the reproduction cycle and energy allocation of the bivalve Macoma balthica (L.) on a tidal flat. Journal of Experimental Marine Biology and Ecology, 129, 199-217.
Hiscock, K., Tyler-Walters, H. & Jones, H., 2002. High level environmental screening study for offshore wind farm developments - marine habitats and species project. Marine Biological Association of the United Kingdom, Plymouth, AEA Technology, Environment Contract: W/35/00632/00/00, pp.
Hutchins, D.A., Stupakoff, I., Hook, S., Luoma, S.N. & Fisher, N.S., 1998. Effects of Arctic temperatures on distribution and retention of the nuclear waste radionuclides 241Am, 57Co and 137Cs in the bioindicator bivalve Macoma balthica. Marine Environmental Research, 45, 17-28.
Langston, W.J., Chesman, B.S., Burt, G.R., Hawkins, S.J., Readman, J. & Worsfold, P., 2003. Characterisation of European Marine Sites. Poole Harbour Special Protection Area. Occasional Publication. Marine Biological Association of the United Kingdom, 12, 111.
Lardicci, C., Ceccherelli, G. & Rossi, F., 1997. Streblospio shrubsolii (Polychaeta : Spionidae): temporal fluctuations in size and reproductive activity. Cahiers de Biologie Marine, 38 (3), 207-214.
Levin, L. & Creed, E., 1986. Effect of temperature and food availability on reproductive responses of Streblospio benedicti (Polychaeta: Spionidae) with planktotrophic or lecithotrophic development. Marine Biology, 92 (1), 103-113.
Lewis, L., Davenport, J. & Kelly, T., 2002b. A study of the impact of a pipeline construction on estuarine benthic invertebrate communities. Estuarine, Coastal and Shelf Science, 55 (2), 213-221.
Long, W.C., Seitz, R.D., Brylawski, B.J. & Lipcius, R.N., 2014. Individual, population, and ecosystem effects of hypoxia on a dominant benthic bivalve in Chesapeake Bay. Ecological Monographs, 84 (2), 303-327.
Madsen, P.B. & Jensen, K., 1987. Population dynamics of Macoma balthica in the Danish Wadden Sea in an organically enriched area. Ophelia, 27, 197-208.
McLusky, D.S.& Allan, D.G., 1976. Aspects of the biology of Macoma balthica (L.) from the estuarine Firth of Forth. Journal of Molluscan Studies, 42, 31-45.
Mitchell, I.M., 2006. In situ biodeposition rates of Pacific oysters (Crassostrea gigas) on a marine farm in Southern Tasmania (Australia). Aquaculture, 257 (1), 194-203.
Moore, J., 1991. Studies on the Impact of Hydraulic Cockle Dredging on Intertidal Sediment Flat Communities. A report to the Nature Conservancy Council from the Field Studies Council Research Centre, Pembroke, Wales, FSC/RC/4/91.
Oertzen, J.A. Von., 1969. Erste Ergebrisse zur experimentellen ökologie von postglazialen Relikten (Bivalvia) der Ostsee. Limnologica (Berlin), 7, 129-137.
Olafsson, E.B., 1986. Density dependence in suspension feeding populations of the bivalve Macoma balthica. A field experiment. Journal of Animal Ecology, 55, 517-526.
Oost, A., Kabat, P., Wiersma, A. & Hofstede, J. (eds.), 2009. Climate. Thematic report no. 4.1. Wilhelmshaven, Germany: Common Wadden Sea Secretariat, Trilateral Monitoring and Assessment Group, pp. 16.
Philippart, C.J., van Aken, H.M., Beukema, J.J., Bos, O.G., Cadée, G.C. & Dekker, R., 2003. Climate‐related changes in recruitment of the bivalve Macoma balthica. Limnology and Oceanography, 48 (6), 2171-2185.
Schueckel, U. & Kroencke, I., 2013. Temporal changes in intertidal macrofauna communities over eight decades: A result of eutrophication and climate change. Estuarine Coastal and Shelf Science, 117, 210-218.
Seitz, R.D., 2011. Gradient effects on structuring of soft-bottom benthic infauna: Macoma balthica and predation, recruitment, and food availability. Journal of Experimental Marine Biology and Ecology, 409 (1-2), 114-122.
Smaal, A., van Stralen, M. & Craeymeersch, J., 2005. Does the introduction of the Pacific oyster Crassostrea gigas lead to species shifts in the Wadden Sea? The comparative roles of suspension-feeders in ecosystems: Springer, 47, 277-289.
Sörlin, T., 1988. Floating behaviour in the tellinid bivalve Macoma balthica (L.). Oecologia, 77, 273-277.
Sornin, J.-M., Feuillet, M., Heral, M. & Deslous-Paoli, J.-M., 1983. Effet des biodépôts de l'huître Crassostrea gigas (Thunberg) sur l'accumulation de matières organiques dans les parcs du bassin de Marennes-Oléron. Journal of Molluscan Studies, 49 (supp12A), 185-197.
Stekoll, M.S., Clement, L.E. & Shaw, D.G., 1980. Sublethal effects of chronic oil exposure on the intertidal clam Macoma balthica. Marine Biology, 57, 51-60.
Tallqvist, M., 2001. Burrowing behaviour of the Baltic clam Macoma balthica: effects of sediment type, hypoxia and predator presence. Marine Ecology Progress Series, 212, 183–191.
Taylor, A.C., 1976. Burrowing behaviour and anaerobisim in the bivalve Arctica islandica. Journal of the Marine Biological Association of the United Kingdom, 56, 95 - 109.
Theede, H., 1984. Physiological approaches to environmental problems of the Baltic. Limnologica (Berlin), 15, 443-458.
Thiel, M., Stearns, L. & Watling, L., 1998. Effects of green algal mats on bivalves in a New England mud flat. Helgoländer Meeresuntersuchungen, 52 (1), 15-28.
Van der Meer, J., Beukema, J.J. & Dekker, R., 2003. Large spatial variability in lifetime egg production in an intertidal Baltic tellin (Macoma balthica) population. Helgoland Marine Research, 56 (4), 274-278.
Vandendriessche, S., Derweduwen, J. & Hostens, K., 2015. Equivocal effects of offshore wind farms in Belgium on soft substrate epibenthos and fish assemblages. Hydrobiologia, 756 (1), 19-35.
Verdelhos, T., Cardoso, P., Dolbeth, M. & Pardal, M., 2011. Latitudinal gradients in Scrobicularia plana reproduction patterns, population dynamics, growth, and secondary production. Marine Ecology Progress Series, 442, 271-283.
Ysebaert, T., Meire, P., Maes, D. & Buijs, J., 1993. The benthic macrofauna along the estuarine gradient of the Schelde estuary. Netherlands Journal of Aquatic Ecology, 27 (2-4), 327-341.
Zuhlke, R. & Reise, K., 1994. Response of macrofauna to drifting tidal sediments. Helgolander Meeresuntersuchungen, 48 (2-3), 277-289.

References: in fine
 V. 
 V. 
 V. 
 V. 
 V.