Tubificoides benedii and other oligochaetes in littoral mud

Summary

UK and Ireland classification

Description

Extreme upper estuarine fine sandy mud, sometimes with a fine sand fraction, in very sheltered conditions and subject to reduced salinity. An anoxic layer is usually present within the upper 3 cm of the sediment. The infaunal community is extremely poor, consisting almost exclusively of oligochaetes, including Tubificoides benedii and, more rarely, Baltidrilus costatus. The only polychaete species that may occur is Capitella capitata, which may be common. The sediment may form steep banks in the upper parts of macro-tidal estuaries or along saltmarsh creeks. Vaucheria species may form a film on the sediment surface along such creeks, and juvenile shore crabs Carcinus maenas may be common. At the very upper end of estuaries, the oligochaetes Limnodrilus spp. and Tubifex tubifex may be found.

There are three oligochaete-dominated upper estuarine mud biotopes. Tben is the most extreme upper estuarine biotope, occurring at the head of estuaries where there is no strong river flow and, hence, conditions are very sheltered and there is a very strong freshwater influence. Further towards the mid-estuary, this biotope may occur at the top of the shore, with Hed.Ol further down. NhomStr occurs furthest towards the mid estuary, or on the lower shore with Hed.Ol and Tben higher up. Green algae such as Ulva spp. may form mats on the surface of the mud during the summer months. (Information from JNCC, 2022). 

Depth range

Upper shore, Mid shore, Lower shore

Additional information

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Sensitivity reviewHow is sensitivity assessed?

Sensitivity characteristics of the habitat and relevant characteristic species

The biotope description and characterizing species is taken from JNCC (2015). The infaunal community characterizing this biotope is species poor, consisting almost exclusively of oligochaetes, including Tubificoides benedii and, more rarely, Baltidrilus costata (formerly Heterochaeta costata). The only polychaete species that may occur is Capitella capitata, which may be common. At the very upper end of estuaries, the oligochaetes Limnodrilus spp. and Tubifex tubifex may be found. The biotope assessments are based on the key characterizing oligochaete species Tubificoides benedii and Baltidrilus costata. The sensitivities of the oligochaetes Limnodrilus spp. and Tubifex tubifex are assessed for the biotope SS.SMu.SMuVS.LhofTtub (available on the MarLIN website) and are considered only generally for this biotope.

The subtidal mud habitat and salinity regime are important factors structuring this biotope and these are specifically considered within the sensitivity assessments where pressures may result in changes to these.

Resilience and recovery rates of habitat

Usually for oligochaetes fertilization is internal and relatively few large eggs are shed directly into a cocoon that is secreted by the worm (Giere & Pfannkuche, 1982).  Asexual reproduction is possible in some species by spontaneous fission (Giere & Pfannkuche, 1982).  The naid oligochaete Panais litoralis can produce asexually producing clones, the rapid rate of increase (18 times population abundance in 3 months, Gillett et al., 2007) allows this species (which is sensitive to high temperatures, hypoxia and is exposed to predation due to shallow burial) to repopulate rapidly when conditions are favourable.  However, few Tubificidae and Enchytraeidae produce asexually (Giere & Pfannkuche, 1982).

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 and Baltidrilus 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). It is dominant, often reaching huge population densities in coastal areas that are enriched in organic matter and is often described as an ‘opportunist’ species adapted to rapid environmental fluctuations and stress (Giere, 2006; Bagheri & McLusky, 1982). However, unlike other opportunist species it has a long lifespan (a few years, Giere, 2006), a prolonged reproductive period from reaching maturity to maximum cocoon deposition and exhibits internal fertilisation with brooding rather than pelagic dispersal. These factors mean that recolonization is slower than for some opportunistic species such as Capitella capitata and nematodes which may be present in similar habitats.

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 colonising 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 layer s in experimentally defaunated patches (4m2)  after 3 weeks (Gamenick et al., 1996).

Resilience assessment. In general there was little information found for Tubificoides benedii and other oligochaetes, but, taking into consideration the information above (particularly Bolam & Whomersley, 2003) , this review considers that the recoverability of this species is generally ‘High’, so that recovery from defaunation is suggested to occur within two years and that therefore, recovery from any impact (resistance is ‘None’,  ‘Low’ or ‘Medium’) is assessed as ‘High’.

NB: The resilience and the ability to recover from human induced pressures is a combination of the environmental conditions of the site, the frequency (repeated disturbances versus a one-off event) and the intensity of the disturbance. Recovery of impacted populations will always be mediated by stochastic events and processes acting over different scales including, but not limited to, local habitat conditions, further impacts and processes such as larval-supply and recruitment between populations. Full recovery is defined as the return to the state of the habitat that existed prior to impact.  This does not necessarily mean that every component species has returned to its prior condition, abundance or extent but that the relevant functional components are present and the habitat is structurally and functionally recognizable as the initial habitat of interest. It should be noted that the recovery rates are only indicative of the recovery potential.

Hydrological Pressures

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Temperature increase (local) [Show more]

Temperature increase (local)

Benchmark. A 5°C increase in temperature for one month, or 2°C for one year. Further detail

Evidence

Deeper burrowing oligochaetes are protected from fluctuations in temperature by the overlaying sediments which dampen changes if poorly drained (Giere & Pfannkuche, 1982).  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.

Increased temperature was found to trigger the onset of reproduction in Baltidrilus costata (studied as Tubifex costatus) in the Thames (Birtwell & Arthur, 1980). This effect was non-lethal and may be beneficial to populations.

Sensitivity assessment. The dominance of Tubificoides spp. when exposed to a heated effluent suggests that this genus would be highly resistant to an increase in temperature at the pressure benchmark. Biotope resistance is therefore assessed as ‘High’ and resilience as ‘High’ (by default), so that the biotope is considered to be ‘Not sensitive’.

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Temperature decrease (local) [Show more]

Temperature decrease (local)

Benchmark. A 5°C decrease in temperature for one month, or 2°C for one year. Further detail

Evidence

Most littoral oligochaetes, including tubificids and enchytraeids, can survive freezing temperatures and can survive in frozen sediments (Giere & Pfannkuche, 1982). Tubificoides benedii (studied as Peloscolex benedeni) recovered after being frozen for several tides in a mudflat (Linke, 1939).

Sensitivity assessment. Based on freezing tolerances of Tubificoides benedii (Linke, 1939) biotope resistance is assessed as ‘High’ to decreases in temperature. Resilience is assessed as ‘High’ (by default) and the biotope is therefore considered to be ‘Not sensitive’.

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Salinity increase (local) [Show more]

Salinity increase (local)

Benchmark. A increase in one MNCR salinity category above the usual range of the biotope or habitat. Further detail

Evidence

This biotope is present in reduced (18-30 ppt) salinity habitats (JNCC, 2015), a change at the pressure benchmark therefore represents a change from reduced to full salinity (30-35 ppt). 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) to low (SS.SMu.SMuVS.LhofTtub) habitats (JNCC,2015). The species characterizing these biotopes are likely to vary. Giere & Pfannkuche (1982) identified how species change over a hypothetical salinity gradient with marine stenohaline species present at full salinities replaced by more euryhaline oligochaete species including Tubificoides benedii and Tubificoides pseudogasterParanais litoralis and Baltidrilus costata (formerly Heterochaeta costata).  Studies in the Rhine delta have found that Tubificoides benedii, is more tolerant of a range of salinities than Baltidrilus costata (as Heterochaeta costata) which preferred shallow water brackish stations (Verdonschot et al. 1982). However, numerous studies suggest that Baltidrilus costata tolerates a wide range of salinities from 1‰ to 28‰ (Giere & Pfannkuche, 1982 and references therein), suggesting that while tolerant of some changes, an increase to full salinity may lead to reductions in abundance of this species.

Sensitivity assessment. Based on the distribution of oligochaetes (including characterizing species) in full, variable and reduced salinity, the biological assemblage associated with the biotope is considered to have ‘High’ resistance  and ‘High’ resilience and is therefore considered to be ‘Not sensitive’, although the biotope classification may revert to a similar, full salinity, oligochaete dominated biotope.

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Salinity decrease (local) [Show more]

Salinity decrease (local)

Benchmark. A decrease in one MNCR salinity category above the usual range of the biotope or habitat. Further detail

Evidence

This biotope is present in reduced (18-30 ppt) salinity habitats (JNCC, 2015), a change at the pressure benchmark therefore represents a change from reduced to low (<18 ppt) salinity. 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).  It is therefore considered that a decrease in salinity at the pressure benchmark would 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. This would result in the loss of the characterizing biotope. 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. A reduction in salinity at the pressure benchmark may lead to species replacement and biotope reclassification to SS.SMu.SMuVS.LhofTtub. Biotope resistance is therefore assessed as ‘Low’ and resilience as ‘High’ (following a return to usual habitat conditions), so that biotope sensitivity is assessed as ‘Low’.

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Water flow (tidal current) changes (local) [Show more]

Water flow (tidal current) changes (local)

Benchmark. A change in peak mean spring bed flow velocity of between 0.1 m/s to 0.2 m/s for more than one year. Further detail

Evidence

Increases and decreases in water velocity may lead to increased erosion or deposition. The associated pressures alteration to sediment type and siltation are assessed separately.  Experimental increases in near-bed current velocity were achieved over intertidal sandflats by placing flumes on the sediment to accelerate water flows (Zuhlke & Reise, 1994). The increased flow led to the erosion of up to 4cm depth of surface sediments.  No significant effect was observed on the abundance of Capitella capitata and numbers of Tubificoides benedii and Tubificoides pseudogaster were unaffected, as they probably avoided suspension by burrowing deeper into sediments. This was demonstrated by the decreased abundance of oligochaetes in the 0-1cm depth layer and increased abundance of oligochaetes deeper in sediments (Zuhlke & Reise, 1994).  A single storm event had a similar result with decreased abundance of oligochaetes in surficial layers, coupled with an increase in deeper sediments (Zuhlke & Reise, 1994). Although Tubificoides spp. can resist short-term disturbances their absence from sediments exposed to higher levels of disturbance indicate that they would be sensitive to longer-term changes in sediment mobility (Zuhlke & Reise, 1994). Birtwell and Arthur (1980) reported seasonal changes in abundance in Baltidrilus costata (as Tubifex costatus) which they attributed to erosion of the upper sediment layers caused by high river flows and wave action.

In the turbid waters of estuaries, where many mud habitats develop, a reduction in water flow is likely to result in a significant increase in siltation increasing the silt and clay content of the substratum. Decreases in water flow with increased siltation of fine particles are considered unlikely to alter the physical character of this habitat type as it is already found in sheltered areas where siltation occurs and where particles are predominantly fine. Reductions in waterflow occurring through the presence of trestles (for off-bottom oyster cultivation) arranged in parallel rows in the intertidal area (Goulletquer & Héral, 1997) reducing the strength of tidal currents (Nugues et al., 1996) has been observed to limit the dispersal of pseudofaeces and faeces in the water column and thus increase the natural sedimentation process by several orders of magnitude (Ottman & Sornin, 1985, summarised in Bouchet & Sauriau, 2008). As the characterizing oligochaetes can live relatively deeply buried and in depositional environments with low water flows (based on habitat preferences) and low oxygenation they are considered to be not sensitive to decreases in water flow.

Sensitivity assessment. Where increased or decreased water flows altered the sediment type this could lead to sediment reclassification, this change is assessed in the sedimentary change assessment. As muds tend to be cohesive and the surface tends to be smooth reducing turbulent flow, an increase at the pressure benchmark may not lead to increased erosion, biotope resistance is assessed as ‘Medium’ as a precautionary assessment, resilience is assessed as ‘High’ (following restoration of usual conditions) and sensitivity is assessed as ‘Low’. The biotope is not considered to be sensitive to decreased flows due to its presence in sheltered habitats and the tolerance of Tubificoides benedii for low oxygen and sediment deposition.

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Emergence regime changes [Show more]

Emergence regime changes

Benchmark.  1) A change in the time covered or not covered by the sea for a period of ≥1 year or 2) an increase in relative sea level or decrease in high water level for ≥1 year. Further detail

Evidence

This biotope is found on the lower shore, mid shore and upper shore (JNCC, 2015). As habitats from the sublittoral to the supralittoral are habitable for tubificds and enchytraeid oligochaetes (Giere, 1993) the biotope is not considered sensitive to changes in emergence that alter emergence periods. The characterizing species are found in subtidal biotopes and a change in tidal regime that led to this biotope becoming permanently submerged would result in biotope reclassification to a biotope such as SS.SMu.SMuVS.OlVS (oligochaetes in variable or reduced salinity infralittoral muddy sediment ).

Sensitivity assessment. The biotope based on the biological assemblage is considered to have ‘High’ resistance to changes in emergence and ‘High’ resilience (by default), so that the biotope is considered to be ‘Not sensitive to this pressure at the benchmark. 

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Wave exposure changes (local) [Show more]

Wave exposure changes (local)

Benchmark. A change in near shore significant wave height of >3% but <5% for more than one year. Further detail

Evidence

This biotope occurs in habitats that are sheltered from strong wave action. Disturbance of sediment by waves may reduce oligochaete abundance (Giere, 1977) and oligochaetes may be absent from very wave exposed shores (Giere & Pfannkuche, 1982 and references therein).  As this biotope occurs across three wave exposure categories; sheltered, extremely sheltered and very sheltered, JNCC (2015), this is considered to indicate that mid-range biotopes would tolerate both an increase or decrease in wave exposure at the pressure benchmark. Resistance is therefore assessed as ‘High’ and resilience as ‘High’ by default and the biotope is considered to be ‘Not sensitive’.

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Chemical Pressures

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Transition elements & organo-metal contamination [Show more]

Transition elements & organo-metal contamination

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed but evidence is presented where available.

Contamination at levels exceeding the pressure benchmark may have negative effects. A 2-year microcosm experiment was undertaken to investigate the impact of copper on the benthic fauna of the lower Tyne Estuary (UK) by Hall & Frid (1995). During a 1-year simulated contamination period, 1 mg l−1copper was supplied at 2-weekly 30% water changes, at the end of which the sediment concentrations of copper in contaminated microcosms reached 411 μg g−1. Toxicity effects reduced populations of the four dominant taxa including Tubificoides spp.). When copper dosage was ceased and clean water supplied, sediment copper concentrations fell by 50% in less than 4 days, but faunal recovery took up to 1 year, with the pattern varying between taxa. Since the copper leach rate was so rapid it is concluded that after remediation, contaminated sediments show rapid improvements in chemical concentrations, but faunal recovery may be delayed taking up to a year.

Rygg (1985) classified Tubificoides spp as highly tolerant species, common at the most copper polluted stations (>200 mg Kg-1) in Norwegian fjords.

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Hydrocarbon & PAH contamination [Show more]

Hydrocarbon & PAH contamination

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed but evidence is presented where available.

In Finland in oligohaline inland waters near an oil refinery, Baltidrilus costata (as Tubifex costatus) appeared to be sensitive to oil pollution and had completely disappeared from sediments exposed to pollution and did not recolonize during a 4year post pollution period (Leppäkoski & Lindström, 1978). Tubificoides benedii appears to be more tolerant and was found in UK waters near oil refineries as the sole surviving member of the macrofauna. Populations were, however, apparently reduced and the worms were absent from areas of oil discharge and other studies indicate sensitivity to oiling (Giere & Pfannkuche, 1982).

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Synthetic compound contamination [Show more]

Synthetic compound contamination

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed but evidence is presented where available.

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Radionuclide contamination [Show more]

Radionuclide contamination

Benchmark. An increase in 10µGy/h above background levels. Further detail

Evidence

No evidence was found for radionuclide uptake by marine oligochaetes.

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Introduction of other substances [Show more]

Introduction of other substances

Benchmark. Exposure of marine species or habitat to one or more relevant contaminants via uncontrolled releases or incidental spills. Further detail

Evidence

This pressure is Not assessed.

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De-oxygenation [Show more]

De-oxygenation

Benchmark. Exposure to dissolved oxygen concentration of less than or equal to 2 mg/l for one week (a change from WFD poor status to bad status). Further detail

Evidence

Oligochaete species vary in their tolerance of hypoxia and associated high sulphide levels. Most enchytraeids and naidids are sensitive to hydrogen sulphide and hypoxia while tubificids are often more resistant (Giere, 2006).

Tubificoides benedii has a high capacity to tolerate anoxic conditions, its extreme oxygen tolerance  is based on an unusually low respiration rate (Giere et al., 1999).  Respiration rates of Tubificoides benedii measured at various oxygen concentrations showed that aerobic respiration is maintained even at very low oxygen concentrations (Giere et al., 1999). Birtwell & Arthur (1980) showed that Tubificoides benedii could tolerate anoxia in the Thames Estuary (LT50 = 58.8 hours at 20oC, 26.6 hours at 25oC  and 17.8 hours at 30oC in experiments with worms acclimated to 20oC.)

Tolerance experiments by Gamenick et al.  (1996) found that Baltidrilus costata (as Heterochaeta costata)  was not affected by hypoxic conditions for at least 3 days but the addition of sulphide 91.96 mmol/litre) caused mortality after 1 day (Gamenick et al., 1996)

Sensitivity assessments. As this biotope is found in intertidal habitats oxygen levels will be recharged during the tidal cycle lowering exposure to this pressure for worms that migrate to surface layers. Based on the reported tolerances for anoxia, biotope resistance is assessed as ‘High’ based on Tubifioides benedii, resilience is assessed as ‘High’ (by default) and the biotope is considered to be ‘Not sensitive’.

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Nutrient enrichment [Show more]

Nutrient enrichment

Benchmark. Compliance with WFD criteria for good status. Further detail

Evidence

In nutrient enriched tidal sediments oligochaetes can dominate assemblages (Gray, 1971; Leppäkoski, 1975; Birtwell & Arthur, 1980). Green algae such as Ulva spp. may form mats on the surface of the mud during the summer months, particularly if nutrient enrichment occurs.

Sensitivity assessment. As the benchmark is relatively protective and would not lead to blooms of Ulva spp. (although green algae may be present on the surface layers of sediments in the summer), biotope resistance is assessed as ‘High’, resilience is assessed as ‘High’ and the biotopeis considered to be ‘Not sensitive’.

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Organic enrichment [Show more]

Organic enrichment

Benchmark. A deposit of 100 gC/m2/yr. Further detail

Evidence

Tubificoides benedii and Baltidrilus costatus are both 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). Their tolerance for organic enrichment is attributed to their adaptation to live in and feed on enriched organic deposits (Pearson & Rosenberg, 1978) and their high population densities in such areas is enhanced by the lack of predation and competition. Tubificoides benedii are abundant in mussel beds (mussel relaying may be the source of smothering) which  has been attributed to their tolerance of organically rich deoxygenated sediment (Commito & Boncavage, 1989). Tubificoides benedii has also been found in elevated abundances in areas of organic enrichment around fish farms (Haskoning, 2006).

Sensitivity assessment. Based on the high tolerance of the characterizing species Tubificoides benedii for organic enrichment, biotope resistance is assessed as ‘High’ and resilience as ‘High’, so that the biotope is considered to be Not sensitive’.

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Not sensitive
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Physical Pressures

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ResistanceResilienceSensitivity
Physical loss (to land or freshwater habitat) [Show more]

Physical loss (to land or freshwater habitat)

Benchmark. A permanent loss of existing saline habitat within the site. Further detail

Evidence

All marine habitats and benthic species are considered to have a resistance of ‘None’ to this pressure and to be unable to recover from a permanent loss of habitat (resilience is ‘Very Low’).  Sensitivity within the direct spatial footprint of this pressure is therefore ‘High’.  Although no specific evidence is described confidence in this assessment is ‘High’, due to the incontrovertible nature of this pressure.

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Physical change (to another seabed type) [Show more]

Physical change (to another seabed type)

Benchmark. Permanent change from sedimentary or soft rock substrata to hard rock or artificial substrata or vice-versa. Further detail

Evidence

The biotope is characterized by the sedimentary habitat (JNCC, 2015), a change to an artificial or rock substratum would alter the character of the biotope leading to reclassification and the loss of the sedimentary community including the characterizing oligochaetes that live buried within the sediment.

Sensitivity assessment. Based on the loss of the biotope, resistance is assessed as ‘None’, recovery is assessed as ‘Very low’ (as the change at the pressure benchmark is permanent and sensitivity is assessed as ‘High’.

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Physical change (to another sediment type) [Show more]

Physical change (to another sediment type)

Benchmark. Permanent change in one Folk class (based on UK SeaMap simplified classification). Further detail

Evidence

Tubificoides benedii (studied as Peloscolex benedeni) are found in a range of substratum types from sandy mixed habitats, fine sands and coarse sands (Giere & Pfannkuche, 1982). Similarly, Baltidrilus costata (asTubifex costatus) is found in mud/silts (Giere & Pfannkuche,1982). Giere & Pfannkuche (1982) suggest that factors that correlate to substratum types such as organic matter availability, size and shape of the intertstitial space between grains, the level of sediment disturbance and water content, rather than the sediment type alone are the key factors influencing distribution.

Sensitivity assessment. A change in sediment type to mixed or coarser particles could lead to changes in the oligochaete community depending on species specific responses. However, if other factors, such as the low salinity, that structure this biotope are not altered, oligochaetes are likely to colonise and a similar biological assemblage could be present (based on the range of sediments Tubificoides benedii inhabits. However, the loss of the littoral mud that characterizes this habitat would change the character of the biotope and is likely to lead to reclassification. For example, a change to sands would likely result in the biotope reverting to the littoral and biotope LS.LSa.MoSa.Ol.VS. Based on a change in character, the biotope is considered to have ‘No’ resistance to this pressure, resilience is assessed as Very ’Low’ as a change at the pressure benchmark is permanent and biotope sensitivity is assessed as ‘High’.

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Habitat structure changes - removal of substratum (extraction) [Show more]

Habitat structure changes - removal of substratum (extraction)

Benchmark. The extraction of substratum to 30 cm (where substratum includes sediments and soft rock but excludes hard bedrock). Further detail

Evidence

Sedimentary communities are likely to be highly intolerant of substratum removal, which will lead to partial or complete defaunation, expose underlying sediment which may be anoxic and/or of a different character or bedrock and lead to changes in the topography of the area (Dernie et al., 2003). Any remaining species, given their new position at the sediment / water interface, may be exposed to conditions to which they are not suited, Removal of 30 cm of surface sediment will remove the oligochaete community and other species present in the biotope. Recovery of the biological assemblage may take place before the original topography is restored, if the exposed, underlying sediments are similar to those that were removed. Hydrodynamics and sedimentology (mobility and supply) influence the recovery of soft sediment habitats (Van Hoey et al. 2008).

Sensitivity assessment. Extraction of 30 cm of sediment will remove the characterizing biological component of the biotope. Resistance is assessed as ‘None’ and biotope resilience is assessed as ’High’.  Biotope sensitivity is therefore ‘Medium’. 

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Abrasion / disturbance of the surface of the substratum or seabed [Show more]

Abrasion / disturbance of the surface of the substratum or seabed

Benchmark. Damage to surface features (e.g. species and physical structures within the habitat). Further detail

Evidence

Tubificoides benedii can be relatively deeply buried and could avoid direct exposure to abrasion although sediment disturbance and compaction could damage these soft-bodied species and oligochaetes in general are not found in high abundances in sediments with high levels of disturbance from wave action.

Experimental studies on crab-tiling impacts have found that densities of Tubificoides benedii and Tubificoides pseudogaster were higher in non-trampled plots (Sheehan et al. 2010), indicating that these oligochaetes have some sensitivity to trampling. Whomersley et al., (2010) conducted experimental raking 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 1 m2 plots were raked twice to a depth of 4cm (using a garden rake). Plots were subject to either low intensity treatments (raking every four weeks) or high (raking every two weeks). The experiment was carried out for 10 months at Creeksea and a year at Blackness. The high and low raking treatments appeared to have little effect on Tubificoides benedii (Whomersley et al., 2010)

Sensitivity assessment. The experiments by Whomersley et al. (2010), suggest that disturbance of the surficial layers has little effect on Tubificoides benedii. Many individuals are likely to be buried more deeply and can migrate to the surface following disturbance, so that little impact is observed through sampling. Abrasion with associated compaction (as in trampling) may have a greater impact. Resistance is therefore assessed as ‘medium’ and resilience as ‘High’ (by default) so that sensitivity is assessed as ‘Low’.

Medium
High
High
High
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High
High
High
High
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Low
High
High
High
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Penetration or disturbance of the substratum subsurface [Show more]

Penetration or disturbance of the substratum subsurface

Benchmark. Damage to sub-surface features (e.g. species and physical structures within the habitat). Further detail

Evidence

Tubificoides benedii can be relatively deeply buried and could avoid direct exposure to penetration and disturbance of upper sediment layers although sediment disturbance and compaction could damage these soft-bodied species and oligochaetes in general are not found in high abundances in sediments with high levels of disturbance from wave action.

Whomersley et al., (2010) conducted experimental raking 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 1 m2 plots were raked twice to a depth of 4cm (using a garden rake). Plots were subject to either low intensity treatments (raking every four weeks) or high (raking every two weeks). The experiment was carried out for 10 months at Creeksea and a year at Blackness. The high and low raking treatments appeared to have little effect on Tubificoides benedii (Whomersley et al., 2010). These results are supported by observations that two experimental passes of an oyster dredge that removed the sediment to a depth of between 15-20 cm did not significantly affect Tubifcoides benedii (EMU, 1992).

Sensitivity assessment. The experiments by Whomersley et al., (2010) and EMU (1992), suggest that penetration and disturbance of the upper surface  has little effect on Tubificoides benedii. Many individuals are likely to be buried more deeply and can migrate to the surface following disturbance, so that little impact is observed through sampling. Resistance is therefore assessed as ‘Medium’ and resilience as ‘High’ so that sensitivity is assessed as ‘Low’.

Medium
High
High
High
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High
High
High
High
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Low
High
High
High
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Changes in suspended solids (water clarity) [Show more]

Changes in suspended solids (water clarity)

Benchmark. A change in one rank on the WFD (Water Framework Directive) scale e.g. from clear to intermediate for one year. Further detail

Evidence

Estuaries where this biotope is found form can be naturally turbid systems due to sediment resuspension by wave and tide action and inputs of  high levels of suspended solids, transported by rivers. The level of suspended solids depends on a variety of factors including: substrate type, river flow, tidal height, water velocity, wind reach/speed and depth of water mixing (Parr et al. 1998). Transported sediment including silt and organic detritus can become trapped in the system where the river water meets seawater. Dissolved material in the river water flocculates when it comes into contact with the salt wedge pushing its way upriver. These processes result in elevated levels of suspended particulate material with peak levels confined to a discrete region (the turbidity maximum), usually in the upper-middle reaches, which moves up and down the estuary with the tidal ebb and flow. Intertidal mudflats depend on the supply of particulate matter to maintain mudflats and the associated biological community is exposed naturally to relatively high levels of turbidity/particulate matter. 

Sensitivity assessment. The biological assemblage characterizing this biotope is infaunal and consists of sub-surface deposit feeders. Increased suspended solids are unlikely to have an impact and resistance is assessed as ‘High’ and resilience as ‘High’, so that the biotope is considered to be ‘not sensitive’. A reduction in suspended solids may reduce deposition and supply of organic matter, resistance to a decrease is therefore assessed as ‘Medium’ as a shift between deposition and erosion could result in the net loss of surficial sediments. A reduction in organic matter as suspended solids could also reduce production within this biotope. Resistance is assessed as ‘Medium’ as over a year the impact may be relatively small and resistance is assessed as ‘High’, following restoration of usual conditions. Biotope sensitivity is therefore assessed as ‘Low’. 

Medium
Low
NR
NR
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High
High
Low
High
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Low
Low
Low
Low
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Smothering and siltation rate changes (light) [Show more]

Smothering and siltation rate changes (light)

Benchmark. ‘Light’ deposition of up to 5 cm of fine material added to the seabed in a single discrete event. Further detail

Evidence

Intertidal mudflats occur in sheltered environments and, in general, are accreting environments meaning that deposition rather than erosion is the dominant process, this means that the assemblages present (primarily deposit feeders) are adapted to natural levels of siltation through life history traits and can withstand burial (by repositioning in sediment or similarly extending tubes or feeding and respiration structures above the sediment surface). At low levels of siltation the high bioturbatory nature of mudflat organisms decreases sensitivity to effects (Elliott et al. 1998) as sediment turnover rates are relatively rapid. Tubificoides live relatively deeply buried and can tolerate periods of low oxygen that may occur following the deposition of a fine layer of sediment. In addition the presence of this species in areas experiencing deposition, such as estuaries, indicate that this species is likely to have a high tolerance to siltation events. 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 4cm 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 20cm 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 of Tubificoides benedii  were found in both burial treatments after one month (Whomersley et al., 2010)..

Sensitivity assessment. The characterizing species Tubificoides benedii is considered to be able to survive under a deposit of fine grained sediment up to 5cm thick and to burrow and reposition within this. The assessment is supported by the burial experiments conducted by Whomersley et al. (2010).

High
High
High
High
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High
High
High
High
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Not sensitive
High
High
High
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Smothering and siltation rate changes (heavy) [Show more]

Smothering and siltation rate changes (heavy)

Benchmark. ‘Heavy’ deposition of up to 30 cm of fine material added to the seabed in a single discrete event. Further detail

Evidence

The pressure benchmark (30 cm deposit) represents a significant burial event and the deposit may remain for some time in a sheltered mudflat. Some impacts on Tubificoides benedii and other characterizing oligochaetes may occur and it is considered unlikely that signficiant numbers of the population could reposition, based on (Bolam, 2011). Placement of the deposit will therefore result in a defaunated habitat until the deposit is recolonized. Biotope resistance is therefore assessed as 'Low' as some removal of deposit and vertical migration through the deposit may occur. Resilience is assessed as 'High' as migration and recolonization of oligochaetes is likely to occur within two years, biotope sensitivity is therefore assessed as 'Low'.

Low
High
Low
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High
High
Low
High
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Low
High
Low
Low
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Litter [Show more]

Litter

Benchmark. The introduction of man-made objects able to cause physical harm (surface, water column, seafloor or strandline). Further detail

Evidence

Not assessed.

Not Assessed (NA)
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Not assessed (NA)
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Not assessed (NA)
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Electromagnetic changes [Show more]

Electromagnetic changes

Benchmark. A local electric field of 1 V/m or a local magnetic field of 10 µT. Further detail

Evidence

A number of studies have investigated the effects of electromagnetic fields on terrestrial oligochaetes, notable earthworms. Some negative effects have been observed e.g. Tkalec et al., 2013. However no evidence was found to support an assessment at the pressure benchmark for the marine oligochaetes that characterize this biotope.

No evidence (NEv)
NR
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No evidence (NEv)
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No evidence (NEv)
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Underwater noise changes [Show more]

Underwater noise changes

Benchmark. MSFD indicator levels (SEL or peak SPL) exceeded for 20% of days in a calendar year. Further detail

Evidence

Not relevant.

Not relevant (NR)
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Not relevant (NR)
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Not relevant (NR)
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Introduction of light or shading [Show more]

Introduction of light or shading

Benchmark. A change in incident light via anthropogenic means. Further detail

Evidence

No evidence was found to assess this pressure. Studentowicz (1936) found that the enchytraeid oligochaete  Enchytraeus albidus, retracted from light, although the worms accumulated at the surface even when illuminated to avoid low oxygen and hydrogen sulpfide.  Giere and Pfannkuche (1982) considered that other enchytraeids and tubificids are likely to react in the same way. As the biological assemblage occurs within the sediment and can be deeply buried (to 10cm or more) this pressure is considered ‘Not relevant’. 

Not relevant (NR)
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Not relevant (NR)
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Not relevant (NR)
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Barrier to species movement [Show more]

Barrier to species movement

Benchmark. A permanent or temporary barrier to species movement over ≥50% of water body width or a 10% change in tidal excursion. Further detail

Evidence

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, as it is for some marine invertebrates that produce pelagic larvae.  The biotope (based on the biological assemblage) is therefore considered to have ‘High’ resistance to the presence of barriers that lead to a reduction in tidal excursion, resilience is assessed as ‘High’ (by default) and the biotope is considered to be ‘not sensitive’.

High
Low
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NR
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High
High
High
High
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Not sensitive
Low
Low
Low
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Death or injury by collision [Show more]

Death or injury by collision

Benchmark. Injury or mortality from collisions of biota with both static or moving structures due to 0.1% of tidal volume on an average tide, passing through an artificial structure. Further detail

Evidence

Not relevant’ to seabed habitats.  NB. Collision by grounding vessels is addressed under ‘surface abrasion.

Not relevant (NR)
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Not relevant (NR)
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Not relevant (NR)
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Visual disturbance [Show more]

Visual disturbance

Benchmark. The daily duration of transient visual cues exceeds 10% of the period of site occupancy by the feature. Further detail

Evidence

Most aquatic oligochaetes have no eyes although a few have simple ocelli (eyspots) which are light receptors. Visual disturbance is not considered relevant to this biotope.

Not relevant (NR)
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Not relevant (NR)
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Not relevant (NR)
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NR
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Biological Pressures

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ResistanceResilienceSensitivity
Genetic modification & translocation of indigenous species [Show more]

Genetic modification & translocation of indigenous species

Benchmark. Translocation of indigenous species or the introduction of genetically modified or genetically different populations of indigenous species that may result in changes in the genetic structure of local populations, hybridization, or change in community structure. Further detail

Evidence

Key characterizing species within this biotope are not cultivated or translocated. This pressure is therefore considered ‘Not relevant’ to this biotope group.

Not relevant (NR)
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Not relevant (NR)
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Not relevant (NR)
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NR
NR
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Introduction or spread of invasive non-indigenous species [Show more]

Introduction or spread of invasive non-indigenous species

Benchmark. The introduction of one or more invasive non-indigenous species (INIS). Further detail

Evidence

The biotope may be exposed to a number of invasive species that can cause impacts. The largest effect may be from species that significantly alter the character of the biotope, such as reef-forming species and invasive vegetation. Commito (1987) found that the population density of Tubificoides benedii was the same or higher in mussel beds than in open areas, suggesting that colonization of sediments by the Pacific oyster Magallana gigas would not necessarily impact the population (although it would alter the character of the biotope). The polychaete Marenzellaria viridis has become established in estuaries in Europe but a recent paper on its impacts where Tubificoides were abundant did not report on oligochaete impacts (Delefosse et al., 2012). Infaunal non-natives may impact the biotope through sediment disturbance, predation or competition for resources, however, no examples were found.

Tang & Kristensen (2010) found that the abundance of macrofauna, including Tubificoides was lower in marsh invaded by the hybrid cordgrass Spartina anglica than in mudflats. Colonization of upper mudflats by this species would alter the character of the biotope resulting in loss and reclassification.

The Pacific oyster, Magallana (syn. Crassostrea) gigas, is native to warm temperate regions from the northwest Pacific to Japan and northeast Asia, including Cape Mariya (Russia) to Hong Kong (China) (Carrasco & Baron, 2010; GBNNSS, 2011, 2012). It is a fast-growing and tolerant species that has become a successful invader in the coastal waters of all continents, aside from Antarctica (Wrange et al., 2010; Carrasco & Baron, 2010; Padilla, 2010). Magallana gigas is recognised as a beneficial and important species in aquaculture worldwide (Padilla, 2010). It was initially introduced for aquaculture in Europe and the UK in the 1960s due to a decline in the Portuguese oyster (Crassostrea angulata) and the European flat oyster (Ostrea edulis) (Spencer et al., 1994; GBNNSS, 2011, 2012; Humphreys et al., 2014 cited in Alves et al., 2021; Hansen et al., 2023).

Since introduction, the species has invaded and established self-sustaining natural populations throughout Europe from the North Sea, Wadden Sea and Scandinavian coastlines to the Atlantic coastlines of Spain and Portugal, as well as the Mediterranean and Adriatic Sea (Wrange et al., 2010; GBNNSS, 2011, 2012; Ezgeta-Balic et al., 2019; Spagnolo et al., 2019; Bergstrom et al., 2021; Hansen et al., 2023). In the UK, the species predominantly occurs around the southern and western coastlines (OBIS, 2024; NBN, 2024). Shipping activity has also been associated with the introduction of Magallana gigas in the northeastern Adriatic Sea, where it was not introduced for aquaculture (Ezgeta-Balic et al., 2019). It was also suggested that some Magallana gigas populations were established in southwest England from France possibly via fouling on ships (GBNNSS, 2011, 2012; Padilla, 2010; Ezgeta-Balic et al., 2019).

Magallana gigas has a high fecundity, a long-lived pelagic larval phase (2 to 4 weeks) and can produce up to 200 million eggs during spawning (Herbert et al., 2012, 2016; Alves et al., 2021; Wood et al., 2021; Hansen et al., 2023). Hence, as a broadcast spawner, it has a high dispersal potential of more than 1000 km (Padilla, 2010; Wood et al., 2021). Larval mortality can be as large as 99%, as larvae are sensitive to environmental conditions (Alves et al., 2021). However, adults are long-lived so populations can survive with infrequent recruitment (Padilla, 2010). Larval dispersal and mass spawning events have facilitated the settlement and establishment of Pacific oysters, as seen in the Oosterschelde estuary, Netherlands (Hansen et al., 2023). It has been suggested that the spread of the Pacific oyster in Scandinavia is due to northward larval drift on tidal and wind-driven currents (Hansen et al., 2023). Wood et al. (2021) suggested that larval dispersal of the Pacific oyster from populations within and outside the UK was possible via unaided (passive) transport by currents, but that aquaculture and offshore structures (e.g. windfarms) increased the risk of the invasive species spreading and the geographical extent of spread.

Magallana gigas is an ecosystem engineer and can dramatically change habitat structure when it invades. Once successfully settled, groups of Pacific oysters may form dense aggregations, potentially forming a reef, which in some regions can reach densities of 700 individuals m2 (Herbert et al., 2012, 2016). Once, the density of live or dead Pacific oysters reaches or exceeds 200 ind./m2 little of the underlying substratum remains visible (Herbert et al., 2016). These reefs can stabilize the sediment surface locally (Troost, 2010). When such reefs are formed or, particularly when the species colonizes soft sediments such as mud or sand, it can change and affect local communities, by creating hard substrata for mobile species, which might not otherwise be present before the invasion (Padilla, 2010). However, Hansen et al. (2023) suggested that no immediate ecosystem risk is observed where the Pacific oyster occurs sporadically.

Magallana gigas has been reported from estuaries growing on intertidal mudflats, sandflats, and other soft sediments (Padilla, 2010; Herbert et al., 2016; Cabral et al., 2020). The settlement of spat on hard substrata within sediments has been observed in the estuaries of the River Dart, Exe, Fal, Fowey, Tamar, Teign, and Yealm in Devon and Cornwall, the Menai Straits, Wales and large estuaries of Lough Swilly, Lough Foyle and the Shannon in Ireland, and the Tagus Estuary in Portugal (Spencer et al., 1994; Kochmann, 2012; Kochmann et al., 2013; Cabral et al., 2020). In Lough Swilly, Lough Foyle and the Shannon, the Pacific oyster was often associated with intertidal mud or sandflats (Kochmann et al., 2013). In contrast, the Pacific oysters were absent from sandflat areas in Poole Harbour (Mckinstry & Jensen, 2013).

Magallana gigas requires hard substrata for successful settlement and establishment, including littoral rock, bedrock, chalk, bare boulders, cobbles and pebbles and shells (Kochmann, 2012; Kochmann et al., 2013; Mckinstry & Jensen, 2013; Herbert et al., 2016; Tillin et al., 2020). It also prefers mudflats with mixed sediment composed of shingle and sand, attaching to whatever hard substrata are available within otherwise unsuitable fine muddy sediment (Spencer et al., 1994; Mckinstry & Jensen, 2013; Tillin et al., 2020).

Although shorelines comprised of mainly mud were suggested to be unsuitable for spat settlement (Spencer et al., 1994), the presence of smaller hard substrata, such as shells or pebbles, can enable larvae to settle (Tillin et al., 2020). For example, in the River Teign estuary, Pacific oyster settlement was observed on shell-covered ground mainly attached to mussel shells, and occasionally attached to cockles, stones and common periwinkle (Littorina littorea) shells on a mud flat in the estuarine intertidal zone otherwise mainly comprised of sand and mud (Spencer et al., 1994). In addition, the Blue Lagoon on the north shore of Poole Harbour had the highest abundance of oysters on mud mixed with shingle and shell (Mckinstry & Jensen, 2013). Outside of the Blue Lagoon, oysters were also recorded on mixed substrata composed of mud, gravel, and shell (McKinstry & Jensen, 2013). In the Wadden Sea, the distribution of Magallana gigas on soft sediment shores can overlap with native bivalve species such as Cerastoderma edule, Macoma balthica and Scrobicularia plana (Troost, 2010; Herbert et al., 2012, 2016). However, these native species are likely to occur at higher shore elevations compared to the lower shore habitats preferred by the Pacific oyster (Troost, 2010; Herbert et al., 2012, 2016). For example, in the Wadden Sea greater densities of Cerastoderma edule and Macoma balthica were found above the level of Magallana gigas reef development (Herbert et al., 2012). Tillin et al. (2020) concluded that while successful invasions occurred on mudflats, Magallana gigas prefers mixed substrata. Fine mud sediments without hard substrata (such as small stones, gravel, and shell) are unlikely to be suitable (Tillin et al., 2020). The speed of Magallana gigas reef formation on soft substrata seems to be dependent on the amount of hard substrata present, developing quicker once there is a sufficient amount (Troost, 2010). Bergstrom et al. (2021) reported that the presence of Magallana gigas was partially dependent on increasing gravel content up to 15% but remained stable with increasing percentages (measured up to 80%).

The oyster reefs, in the Wadden Sea and Brittany, on littoral muddy and sandy habitats formed predominantly at lower tidal levels from Mean Low Water levels to the shallow subtidal (Troost, 2010; Herbert et al., 2012, 2016). Pacific oyster spatfall was recorded in the estuarine intertidal zone on areas with hard substrata of stone and shell, particularly between the low water of spring tides and high water of neap tides, such as in the Menai Strait (Spencer et al., 1994).

At high densities the Pacific oyster reef smothers sediment, provides hard substrata in an otherwise sedimentary environment with additional niches for colonization by other species that require hard substratum (e.g. barnacles), and changes surface roughness and local hydrography (Troost, 2010; Herbert et al., 2012, 2016; Tillin et al., 2020). Lejart & Hily (2011) found the surface available for epibenthic species in the Bay of Brest, increased 4-fold when oysters were present on mud, for every 1 m2 of colonized substrata the oyster reef added 3.87 m2 of surface area on mud sediment. An increase in available settlement substrata, free of epibiota, could be the reason oyster reefs see an increase in macrofaunal abundance. This can change the community composition and habitat structure in reefs on soft mud sediments, creating new habitats for an increasing abundance of infaunal and epibenthic mobile species (Kochmann et al., 2008; Lejart & Hily, 2011; Zwerschke et al., 2018). Results have shown 38% of species present in the oyster reefs on mud were characteristic of rocky substratum habitats (Lejart & Hily, 2011).

In the Bay of Brest, Pacific oyster reefs had a higher diversity and species richness than surrounding mud habitats, including the mud underneath the reefs, where the population was dominated by carnivores rather than suspension the feeders found on the mudflats (Lejart & Hily, 2011; Herbert et al., 2012). In addition, in muddy habitats around the UK, Ireland and Northern France, macrofaunal diversity increased as Pacific oyster density increased but epifaunal diversity decreased as oyster densities increased (Zwerschke et al., 2018). It was suggested that the decrease in epifaunal diversity was due to a decrease in settlement space and an increase in habitat fragmentation because of dense oyster assemblages (Zwerschke et al., 2018).

Green & Crowe (2014) examined the effects of Magallana gigas density in experimental plots (0.25 m2) in Lough Swilly and Lough Foyle, Ireland. The number of species and species diversity increased with oyster cover on mudflats, depending on site and duration. The assemblage also changed due to the increased abundance of barnacles and bryozoans on the oyster shells and polychaetes within the sediment (Green & Crowe, 2014). Zwerschke et al. (2020) suggested that Pacific oyster beds could replace the ecosystem services provided by native oysters, in areas where native oysters had been lost. Morgan et al. (2021) suggested that the smothering of sediment habitats could prevent fish and bird species from feeding on infauna like worms, molluscs, and crustaceans. Also, the development of tidepools within mixed Pacific oyster and blue mussel reefs in soft sediment intertidal sites has been observed in the Wadden Sea, which can create new microhabitats within the reefs (Weniger et al., 2022).

Pacific oysters have been found to reduce the proportion of fine particles and increase the proportion of large particles in the mud under the reef (Lejart & Hily, 2011). The evidence suggests that Pacific oyster reefs change sediment characteristics, by affecting nutrient cycling and increasing the organic content of sediment, sand-to-silt ratio and levels of porewater ammonium (Kochmann et al., 2008; Padilla, 2010; Wagner et al., 2012 cited in Tillin et al., 2020; Green & Crowe, 2014; Herbert et al., 2012, 2016; Zwerschke et al., 2020; Hansen et al., 2023).  Zwerschke et al. (2020) found no significant differences in nutrient cycling rates of native oyster beds or Magallana gigas beds or their associated benthic communities, in experimental plots in Ireland. Persistent changes in the rates of nutrient cycling were driven by the density and presence of oysters (Zwerschke et al., 2020).

The deposition of faeces and pseudo-faeces by Magallana gigas can increase the toxic levels of sulphide in sediments and associated hypoxic sediment conditions, which can reduce photosynthesis and growth in eelgrass (Kelly & Volpe, 2007). Faecal deposition and hypoxia have also been suggested to explain a reduction in species diversity in the sediment underlying high-density oyster reefs (Green & Crowe, 2013, 2014; Herbert et al., 2016). However, Lejart & Hily (2011) observed no organic or silt enrichment by Pacific oysters in mud beneath oyster reefs in the Bay of Brest, and no significant difference in the amount of organic matter found in the mud underneath oyster reefs and on bare mud not colonized by the oyster. The biodeposits excreted by the oyster may be washed away by powerful tides and currents seen in the Bay of Brest and the effects of organic enrichment at oyster reefs might be minimal due to wave action (Lejart & Hily, 2011).

The American slipper limpet Crepidula fornicata was introduced to the UK and Europe in the 1870s from the Atlantic coasts of North America with imports of the eastern oyster Crassostrea virginica. It was recorded in Liverpool in 1870 and the Essex coast in 1887-1890. It has spread through expansion and introductions along the full extent of the English Channel and into the European mainland (Blanchard, 1997, 2009; Bohn et al., 2012, 2013a, 2013b, 2015; De Montaudouin et al., 2018; Helmer et al., 2019; Hinz et al., 2011; McNeill et al., 2010; Powell-Jennings & Calloway, 2018; Preston et al., 2020; Stiger-Pouvreau & Thouzeau, 2015).

Crepidula fornicata is recorded from shallow, sheltered bays, lagoons and estuaries or the sheltered sides of islands, in variable salinity (18 to 40) although it prefers ca 30 (Tillin et al., 2020). Larvae require hard substrata for settlement. It prefers muddy gravelly, shell-rich, substrata that include gravel, or shells of other Crepidula, or other species e.g., oysters, and mussels. It is highly gregarious and seeks out adult shells for settlement, forming characteristic ‘stacks’ of adults. But it also recorded in a wide variety of habitats including clean sands, artificial substrata, Sabellaria alveolata reefs and areas subject to moderately strong tidal streams (Blanchard, 1997, 2009; Bohn et al., 2012, 2013a, 2013b, 2015; De Montaudouin et al., 2018; Hinz et al., 2011; Powell-Jennings & Calloway, 2018; Preston et al., 2020; Stiger-Pouvreau & Thouzeau, 2015; Tillin et al., 2020).

High densities of Crepidula fornicata cause ecological impacts on sedimentary habitats. The species can form dense carpets that can smother the seabed in shallow bays, changing and modifying the habitat structure. At high densities, the species physically smothers the sediment, and the resultant build-up of silt, pseudofaeces, and faeces is deposited and trapped within the bed (Tillin et al., 2020, Fitzgerald, 2007, Blanchard, 2009, Stiger-Pouvreau & Thouzeau, 2015). The biodeposition rates of Crepidula are extremely high and once deposited, form an anoxic mud, making the environment suitable for other species, including most infauna (Stiger-Pouvreau & Thouzeau, 2015, Blanchard, 2009). For example, in fine sands, the community is replaced by a reef of slipper limpets, that provide hard substrata for sessile suspension-feeders (e.g., sea squirts, tube worms and fixed shellfish), while mobile carnivorous microfauna occupy species between or within shells, resulting in a homogeneous Crepidula dominated habitat (Blanchard, 2009). Blanchard (2009) suggested the transition occurred and became irreversible at 50% cover of the limpet. De Montaudouin et al. (2018) suggested that homogenization occurred above a threshold of 20-50 Crepidula /m2.

Impacts on the structure of benthic communities will depend on the type of habitat that Crepidula colonizes. De Montaudouin & Sauriau (1999) reported that in muddy sediment dominated by deposit-feeders, species richness, abundance and biomass increased in the presence of high densities of Crepidula (ca 562 to 4772 ind./m2), in the Bay of Marennes-Oléron, presumably because the Crepidula bed provided hard substrata in an otherwise sedimentary habitat. In medium sands, Crepidula density was moderate (330-1300 ind./m2) but there was no significant difference between communities in the presence of Crepidula. Intertidal coarse sediment was less suitable for Crepidula with only moderate or low abundances (11 ind./m2) and its presence did not affect the abundance or diversity of macrofauna. However, there was a higher abundance of suspension–feeders and mobile Crustacea in the absence of Crepidula (De Montaudouin & Sauriau, 1999). The presence of Crepidula as an ecosystem engineer has created a range of new niche habitats, reducing biodiversity as it modifies habitats (Fitzgerald, 2007). De Montaudouin et al. (1999) concluded that Crepidula did not influence macroinvertebrate diversity or density significantly under experimental conditions, on fine sands in Arcachon Bay, France. De Montaudouin et al. (2018) noted that the limpet reef increased the species diversity in the bed, but homogenised diversity compared to areas where the limpets were absent. In the Milford Haven Waterway (MHW), the highest densities of Crepidula were found in areas of sediment with hard substrata, e.g., mixed fine sediment with shell or gravel or both (grain sizes 16-256 mm) but, while Crepidula density increased as gravel cover increased in the subtidal, the reverse was found in the intertidal (Bohn et al., 2015). Bohn et al. (2015) suggested that high densities of Crepidula in high-energy environments were possible in the subtidal but not the intertidal, suggesting the availability of this substratum type is beneficial for its establishment. Hinz et al. (2011) reported a substantial increase in the occurrence of Crepidula off the Isle of Wight, between 1958 and 2006, at a depth of ca 60 m, on hard substrata (gravel, cobbles, and boulders), swept by strong tidal streams. Presumably, Crepidula is more tolerant of tidal flow than the oscillatory flow caused by wave action which may be less suitable (Tillin et al., 2020).

The availability of hard substrata (e.g., gravel) may only restrict initial colonization as higher densities of Crepidula function as substrata for subsequent colonization (Thieltges et al., 2004; Blanchard, 2009). However, Bohn et al. (2015) noted that Crepidula occurred at low density or was absent in areas of homogenous fine sediment and areas dominated by boulders. Bohn et al. (2015) suggested that wave action (exposure) probably prevented the establishment of large numbers of Crepidula in high-energy areas. Blanchard (2009) noted that sandy areas in the Bay of Saint-Mont Michel were not colonized by Crepidula because of surface sand mobility. Thieltges et al. (2003) also noted that storm events removed some clumps of mussels and presumably Crepidula onto tidal flats where they disappeared, which caused their abundance to fluctuate. Similarly, Crepidula was absent from sandy substrata in Swansea Bay but was most abundant in the shelter of the breakwater at the Swansea east site (Powell-Jennings & Calloway, 2018). Powell-Jennings & Calloway (2018) noted that Crepidula is killed by sudden burial and possibly burial due to deposition, which could mitigate Crepidula density. In addition, in the MHW, the highest densities of Crepidula were found in areas of sediment with hard substrata, e.g., mixed fine sediment with shell, or gravel or both but, while Crepidula density increased as gravel cover increased in the subtidal, the reverse was found in the intertidal (Bohn et al., 2015). However, gravel formed the base of most stacks of Crepidula in the intertidal, which suggested that initial colonization occurred on available hard substrata (i.e., gravel) in the absence of adult shells of Crepidula (Bohn et al., 2015). 

Crepidula is recorded from the lower intertidal to ca 160 m in depth but it is most common in the shallow subtidal and low water springs (Blanchard, 1997; Thieltges et al., 2003; Bohn et al., 2012, 2015; Hinz et al., 2011; OBIS, 2023; Tillin et al., 2020). Bohn et al. (2012, 2013a, 2013b, 2015) suggested that extreme conditions in intertidal limited its upward distribution due to early post-settlement mortality. It reached its highest densities on the lower shore (below ca 0.7 m) and was absent from the high tidal level (ca 1.8 m) in the MHW (Bohn et al., 2015). Bohn et al. (2013b) noted that Crepidula spat in their experimental intertidal panels suffered high mortality of 78-100% during emersion by low water spring tides. Thieltges et al. (2003) noted that Crepidula abundance at the intertidal to the subtidal transition zone (ca 21/ m2) was significantly higher than in the upper, mid, and lower intertidal ca <3/ m2). Similarly, Diederich & Pechenik (2013) noted that Crepidula densities were not significantly different in the low intertidal (+0.2 m) and shallow subtidal (-1 m) but became lower at +0.4 and were absent above +0.6 m in Bissel Cove, Rhode Island where the mean high water was +1.38 m. They reported that intertidal adults experienced temperatures of ca 42°C, which were 15°C higher than subtidal adults. However, there was no significant difference in the tolerance of subtidal and intertidal adults with a lethal range of 33-37°C after three hours in the laboratory. Diederich & Pechenik (2013) suggested that adult Crepidula were living close to their upper thermal limit in Rhode Island and would be driven into the subtidal due to climate change. Diederich et al. (2015) reported that most juvenile Crepidula died after aerial exposure under laboratory conditions (20°C, 75% relative humidity), while adults from the intertidal and subtidal survived (26°C, 75% relative humidity). Franklin et al. (2023) noted that the body mass index of adult Crepidula did not decrease significantly in winter months in New Hampshire, USA, but did decrease in spring and summer, probably due to its investment in reproduction. 

The density of Crepidula populations in northern Europe (Germany, Denmark, and Norway) was significantly lower (ca <100/ m2) than in southern waters. Thieltges et al. (2004) reported that the population of Crepidula was affected strongly by cold winters in the Wadden Sea. The winters of 2001 and 2003 resulted in ca 56-64% mortality of intertidal Crepidula and up to 97% on one mussel bed, compared to only 11-14% in southern areas without frost. Crepidula almost vanished from the Wadden Sea after the 1978/79 winter and took ten years to recover due to moderate winters which regularly affected the population. Similarly, 25% mortality was observed in Crepidula populations on the south coast of the UK after the extreme 1962/63 winter (Crisp, 1964, Bohn et al., 2012). Thieltges et al. (2003) suggested that global warming may allow Crepidula populations to become more abundant in northern Europe.

Sensitivity assessment. The biotope may be sensitive to invasion by Spartina anglica which would alter the character of the mudflat and the biological assemblage. In addition, the above evidence suggests that this biotope is unsuitable for the colonization of Crepidula fornicata due to a lack of gravel, shells, or any other hard substrata used for larvae settlement (Tillin et al., 2020). Despite the sheltered to extremely sheltered conditions of the habitat that would otherwise be suitable for Crepidula, the mobility of the sediment is unsuitable and makes it unlikely for Crepidula to become established. There may be higher densities of Crepidula in the lower shore examples of the biotope, but the densities may be lower in the mid-shore, and it may be absent from the upper shore due to the unsuitable extreme conditions in the intertidal zone preventing Crepidula post-settlement recruitment and mitigating colonization (Bohn et al. 2015). In addition, the reduced salinity levels in this biotope might prevent colonization at high densities, because the majority of evidence records of Crepidula occur in salinities from 30-35 psu (OBIS, 2023). In addition, Powell-Jennings & Calloway (2018) noted that Crepidula is killed by sudden burial and possibly burial due to deposition, which could mitigate Crepidula density. Therefore, resistance to colonization by Crepidula fornicata, is assessed as 'High' and resilience as 'High' so the biotope is assessed as 'Not sensitive'. The confidence in the assessment is 'Low' because the sensitivity of this biotope to Crepidula is potentially site-specific, there is a risk of its introduction by artificial means, and the is a lack of direct evidence of Crepidula being reported to occur in the biotope.

The above evidence suggests that this biotope is unsuitable for the colonization of Magallana gigas due to a lack of gravel, shells, or any other hard substrata required for successful settlement and establishment (Kochmann, 2012; Kochmann et al., 2013; Mckinstry & Jensen, 2013; Herbert et al., 2016; Tillin et al., 2020). The mid-shore and upper-shore extent of this biotope is not suitable for colonization of the Pacific oyster, which is found predominantly at the Mean Low Water levels to shallow subtidal in sedimentary habitats (Troost, 2010; Herbert et al., 2012, 2016).  Therefore, resistance to colonization by Magallana gigas is assessed as 'High' due to the lack of hard substrata in this biotope. Hence, resilience is assessed as 'High', so this biotope is assessed as 'Not sensitive'. The confidence in the assessment is 'Low' because the sensitivity of this biotope to Magallana gigas is potentially site-specific and there is a risk of its introduction by artificial means. 

However, colonization of the upper shore by Spartina anglica may result in the loss of the characterizing infauna inc. including Tubificoides but this is likely to affect the upper shore extent of the biotope only. Therefore, resistance to colonization by Spartina anglica is assessed as 'Medium' and resilience as 'Very low' so the biotope is assessed as 'Medium'. The confidence in this assessment is 'Low' due to the lack of evidence. 

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Introduction of microbial pathogens [Show more]

Introduction of microbial pathogens

Benchmark. The introduction of relevant microbial pathogens or metazoan disease vectors to an area where they are currently not present (e.g. Martelia refringens and Bonamia, Avian influenza virus, viral Haemorrhagic Septicaemia virus). Further detail

Evidence

Marine oligochaetes host numerous protozoan parasites without apparent pathogenic effects even at high infestation levels  (Giere & Pfannkuche, 1982 and references therein)

Sensitivity assessment. Based on the lack of evidence for mass mortalities in oligochaetes from microbial pathogens, resistance is assessed as ‘High’ and resilience as ‘High’, by default, so that the biotope is assessed as ‘Not sensitive’.

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Removal of target species [Show more]

Removal of target species

Benchmark. Removal of species targeted by fishery, shellfishery or harvesting at a commercial or recreational scale. Further detail

Evidence

No characterizing species within the biotope are targeted by commercial or recreational fishers or harvesters. This pressure is therefore considered ‘Not relevant’. The physical disturbance associated with harvesting other species or accessing fishing and harvesting areas is assessed through the physical disturbance pressures. In estuaries bait digging may occur for Arenicola marina or ragworms (Nephtys spp.). Carcinus maenas may also be harvested, Sheehan (2007) and Sheehan et al. (2010), have studied the disturbance associated with this activity.

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Not relevant (NR)
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Not relevant (NR)
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Removal of non-target species [Show more]

Removal of non-target species

Benchmark. Removal of features or incidental non-targeted catch (by-catch) through targeted fishery, shellfishery or harvesting at a commercial or recreational scale. Further detail

Evidence

Incidental removal of the characterizing species would alter the character of the biotope and the delivery of ecosystem services such as secondary production and bioturbation. Populations of oligochaetes provide food for macroinvertebrates fish and birds. For example up to 67% of flounder and plaice stomachs examined from the Medway estuary (UK) (Van den Broek, 1978) contained the remains of Tubificoides benedii (studied as Peloscolex benedeni) and shrimps which in turn support higher trophic levels (predatory birds and fish). For some migratory birds the characterizing species Tubificoides benedii can form an important part of the diet during winter (Bagheri & McLusky, 1984). Polychaetes and crustaceans are also predators of oligochaetes and may significantly reduce numbers (Giere & Pfannkuche, 1982 and references therein). The loss of the oligochaete population could, therefore,  impact other trophic levels.

Sensitivity assessment. Removal of the characterizing species would alter the character of the biotope. Resistance is therefore assessed as ‘Low’ and resilience as ‘High’ so that sensitivity is categorised as ‘Low’.

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Citation

This review can be cited as:

Tillin, H.M., Lloyd, K.A., & Watson, A., 2024. Tubificoides benedii and other oligochaetes in littoral mud. In Tyler-Walters H. Marine Life Information Network: Biology and Sensitivity Key Information Reviews, [on-line]. Plymouth: Marine Biological Association of the United Kingdom. [cited 03-10-2024]. Available from: https://www.marlin.ac.uk/habitat/detail/1093

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