Limnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment

Researched byGeorgina Budd Refereed byThis information is not refereed.
EUNIS CodeA5.327 EUNIS NameLimnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment

Summary

UK and Ireland classification

EUNIS 2008A5.327Limnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment
EUNIS 2006A5.327Limnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment
JNCC 2004SS.SMu.SMuVS.LhofTtubLimnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment
1997 BiotopeSS.IMU.EstMu.LimTtubLimnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment

Description

Upper estuary muddy sediments with very low fluctuating salinity, characterized by oligochaetes Limnodrilus hoffmeisteri and Tubifex tubifex. This biotope is found in the transitional zone between the freshwater and brackish environments where tidal currents are sufficiently reduced to allow the deposition of fine silt and the establishment of an infaunal community. The biotope contains elements of both freshwater and brackish communities and may be found adjacent to IGS.NeoGam (Neomysis integer and Gammarus spp. in low salinity infralittoral mobile sand), away from the stronger tidal streams. It is similar to IMU.Tub (Tubificoides spp. in reduced salinity infralittoral muddy sediment), although the latter lacks the freshwater element. (Information taken from the Marine Biotope Classification for Britain and Ireland, Version 97.06: Connor et al., 1997a, b).

Recorded distribution in Britain and Ireland

Recorded in upper estuary cohesive mud in the Forth, Thames, Usk and Wye estuaries.

Depth range

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Habitat review

Ecology

Ecological and functional relationships

  • Interstitial salinity is an important factor determining the occurrence of the IMU.LimTtub community. Although tidal, the uppermost part of an estuary may predominantly experience freshwater conditions and this is the case over the first 16 km of the Forth estuary from Stirling, Scotland. Over the first 10 km interstitial salinity is low, is always less than 1psu; at 10 km it is between 1 -1.9 psu, and at 16 km it is between 1.6-4.1psu (McLusky et al., 1981). The infauna consists exclusively of the fresh water oligochaetes, Limnodrilus hoffmeisteri and Tubifex tubifex. Stczynska-Jurewicz (1972) reported that the maximum salinity at which Tubifex tubifex could survive was 9 psu and the maximum at which natural egg laying and development occurred was 4 psu. Kennedy (1965) stated that salinity controlled the distribution of Limnodrilus hoffmeisteri, but gave no precise limits. McLusky et al. (1981) found Tubifex tubifex in localities with a maximum salinity of 4.1 psu, and Limnodrilus hoffmeisteri occurred at salinities of up to 7.7 psu.
  • To a certain extent, the distribution of Gammarus species is also correlated with salinity. Distinct zonation patterns may be observed, Gammarus salinus prefers intermediate salinities, whilst Gammarus zaddachi and Gammarus duebeni predominantly live in more dilute brackish waters, locally penetrating into freshwater transition zones (Bulnheim, 1984).
  • Changes are also apparent in the infaunal species composition in the upper estuary, their relative trophic importance and to a more variable degree their community importance (Diaz, 1979). For instance, oligochaetes are the primary sediment burrowers and bioturbators in freshwater and very low salinity environments owing to the virtual exclusion of polychaetes (which dominate the estuarine infauna) (Diaz, 1979). Tubificids ingest sediment and derive the bulk of their nutrition from bacteria (Brinkhurst & Chuan, 1969; Wavre & Brinkhurst, 1971) and perhaps from algae (Moore, 1978b). Consequently, when large densities of oligochaetes occur (e.g. 127,400 m² at the most densely populated site, in the Forth estuary (McLusky et al., 1981) they have a significant effect upon sedimentary structure through their subsurface ingestion of sediments and surface egestion. Davis (1974) found that feeding and subsequent movement of sediment to the surface occurred mainly at 3-4 cm depth, but small amounts of sediment from as deep as 8-9 cm could also be transported to the surface.
  • The work of Alsterberg (1925) (incomplete citation in Birtwell & Arthur, 1980) indicated that in any 24 hour period Tubifex tubifex and Limnodrilus hoffmeisteri displace a quantity of mud four times greater than their body weight. Appleby & Brinkhurst (1970) found the amount to be greater at higher temperatures, about eight times the body weight. Birtwell & Arthur (1980) considered that such activity could influence the oxygen concentration of the environment as, by bringing sediments of a 'reduced' nature to the surface and into contact with oxygenated water rapid biological and chemical oxidation of organic matter would proceed. Whilst this would increase the oxygen demand of the environment, the anoxic layer may remain at depth (Birtwell & Arthur, 1980).
  • Owing to their feeding method oligochaetes may mediate the passage of heavy metals from contaminated sediment to fish (Patrick & Loutit, 1976; 1978). Several other predators feed upon aquatic oligochaetes other than fish, including leeches, ducks and a variety of invertebrates such as chironomids (Brinkhurst, 1982).
  • Limnodrilus hoffmeisteri competes with Tubifex tubifex in very polluted environments, its abundance being related to the organic content of the sediments and it may dominate the population (Poddubnaya, 1980).
  • The activity of tubificids also affects the stability of surface layers of sediment as they loosen the sediment and render the surface layers susceptible to scour. When sediment scour occurs, fine sediment particles and organic matter are carried into suspension and the resulting oxygen demand is high (HMSO, 1964; Edwards & Rolley, 1965).

Seasonal and longer term change

  • Differences, sometimes distinctly seasonal, may be observed in the breeding period of characterizing oligochaete species according to variation in local conditions, especially temperature, organic enrichment of the sediment and population density (see recruitment processes).
  • The amphipod Gammarus zaddachi conducts extensive migrations along estuaries, it may be found near the limit of tidal influence in winter but moves to more downstream reaches (where reproduction occurs) in spring. A return migration then takes place, primarily by juveniles, until the seaward areas are depopulated in winter (Hough & Naylor, 1992).
  • Habitat structure and complexity

    The substratum consists of cohesive muds which have little inherent structural complexity. Some structural complexity is provided by the burrows of infauna although these are generally simple. Species living within the sediment are likely to be limited to the area above the anoxic layer, the depth of which will vary depending on sediment particle size, organic content and influence of the biotic community (see ecological relationships).

    Productivity

    Productivity in the biotope is expected to be high. Production in IMU.LimTtub is mostly secondary, derived from detritus and organic material. Food becomes available to deposit feeders by sedimentation on the substratum surface. The sediment in the biotope may be nutrient enriched due to proximity to anthropogenic nutrient sources such as sewage outfalls or eutrophicated rivers. In such instances, the species may be particularly abundant. For example, in their study of domestic and industrial pollution, McLusky et al. (1980) found the heavily industrialised, upper Forth estuary, Scotland, in its most polluted sections to be inhabited solely by Tubifex tubifex and Limnodrilus hoffmeisteri. The mean number of these species at the most densely populated site reached 127,400 m² for Tubifex tubifex and 105,800 m² for Limnodrilus hoffmeisteri respectively, with mean biomass of 57.663 and 22.154 g dry wt m² respectively. McLusky et al. (1981) used the P:B ratio of 3:1 for oligochaetes calculated by Haka et al. (1974) and Giere (1975) to give an estimation of the production of oligochaetes on the upper Forth estuary to be 83.91 g/dry wt/m²/yr. These oligochaete species represent a major pathway for the transfer of energy from the sediment to secondary consumers.

    Recruitment processes

    Oligochaetes are hermaphroditic and posses distinct and complex reproductive systems, including permanent gonads. Free spawning and indirect larval development do not occur in the Oligochaeta and would not be especially successful within the typical environment in which oligochaetes occur (cohesive muds). The success of oligochaete species is reliant upon contact mating, exchange of sperm and direct development. The higher survival rate of zygotes produced by such reproduction merits the high parental investment. Furthermore, hermaphroditism is one way for relatively immobile species, who might encounter sexual partners infrequently, to increase their reproductive output, and self fertilization is also a possibility (Brusca & Brusca, 1990). During copulation the mating worms align themselves side-by-side, but face opposite directions so that the male gonopores of one are aligned with the spermathecal openings of the other. Sperm is mutually exchanged and following separation, each functions as an inseminated female. Fertilization occurs in a cocoon (a sheet of mucus produced around the clitellum and all anterior segments) which once formed moves towards the anterior end of the oligochaete by a backward muscular motion of the body. The cocoon is sealed as it passes off the end of the body and it is deposited in benthic debris. Development of the zygote is direct (no larval stage) and time may vary from a week to several months depending on the species and environmental conditions. In climates were relatively severe conditions development time is sufficient to ensure that juveniles hatch in the spring, while in more stable conditions, development time may be shorter and less seasonal (Brusca & Brusca, 1990). More detailed accounts of the recruitment processes of characterizing species follows below, and information is largely based on research by Poddubnaya (1980), who studied the life cycles of several species of tubificid.
    Tubifex tubifex:
    The embryonic period in Tubifex tubifex at various temperatures (2-30°C) lasts from 12 to 60 days, with high mortality observed at temperatures below 10°C and above 20°C. in the earliest stages of development embryos are especially sensitive to changes in dissolved oxygen concentrations between 2-7°C, whilst normal development proceeds between 6-19°C at a dissolved oxygen concentration of 2.5-7 mg/O2/L. After 12-15 days the juvenile worms hatch (3 mm in length, 0.08 mg on average) and their course of maturation is influenced by environmental conditions and population density (which is itself influenced by the productivity of the habitat, e.g. enriched by organic pollution). At 20°C and a population density of < 20000 m², Tubifex tubifex attains maturity within two months, however, lower water temperature (2°C) and higher population density (> 70000 m²) delay maturation by up to 10 months (Poddubnaya, 1980). Duration of the reproductive period varies and is influenced by water temperature, dissolved oxygen concentration and population density. The intensity of reproduction also varies within the year. Mass laying of cocoons in spring and winter alternates with a sudden abatement or halt of sexual activity in summer and autumn and individuals are capable of sexual activity for 3-4 months without interruption. Cocoons laid in winter (January-February) hatch in April, and go on to reproduce once within the first year, during the second year each individual reproduces twice. A fourth period of reproduction is possible in the third year of life, but the life cycle of the species typically lasts between 2-2.5 years (Poddubnaya, 1976).
    Limnodrilus hoffmeisteri:
    Observations on the life cycle of Limnodrilus hoffmeisteri in Estonian and English water bodies and in Upper Volga reservoirs indicate a great plasticity and dependence of the life cycle upon local conditions (organic enrichment, temperature, population density) (Timm, 1962; Kennedy, 1966; 1966b; Poddubnaya, 1980). Breeding activity is possible throughout the year, although peaks are apparent but they occur in different months in different localities, e.g. in the River Thames greatest activity occurs between December and July (Kennedy, 1966). The embryonic period lasts between 15-75 days, with normal development occurring within a temperature range of 10-25°C and at dissolved oxygen concentration of 2.5-10 mg/O2/L. High mortality of embryos occurs in cocoons at low (2-5°C) and high (30°C) temperatures. Like those of Tubifex tubifex, the embryos are especially sensitive to variations in dissolved oxygen concentration and to low temperatures. The worms mature as early as two months and reproduce within their first year, although maturation may be delayed by low or high temperatures (1-4°C and > 30°C) and high population density (> 35000 m²). In the organically enriched River Thames and Shropshire Union canal , Limnodrilus hoffmeisteri bred throughout the year, but with increased activity in winter and spring, but in less productive habitats the species commenced breeding only after it was a year old and the breeding period was shorter and more seasonal (Kennedy, 1966). Potter & Learner (1974) suggested that Limnodrilus hoffmeisteri could produce four or five generations a year in a small Welsh reservoir with a temperature 17-18.6 °C over four months, whereas Ladle (1971) reported the species to produce only a single generation. The whole life cycle of Limnodrilus hoffmeisteri is completed within 2-3 years.
    Gammarus species:
    Sexes are generally separate and species show precopula behaviour, during which the male holds the female using its gnathopods, and carries her for some days before mating. Fertilization is external with sperm being deposited in a brood chamber formed of brood plates that arise from the base of thoracic appendages (Fish & Fish, 1996). Gammarus salinus produces two generations per year. Mature females are present in the population between late November through to July, but the main period of reproduction occurs over the winter (Leineweber, 1985).

    Time for community to reach maturity

    Following successful hatching of juveniles, important characterizing oligochaete species (Limnodrilus hoffmeisteri and Tubifex tubifex) are able to reproduce within a year, and proceed to produce more than one generation in the second year of life. Thus within a period of five years, several generations will have reproduced and a population established. However, in terms of the species present the biotope may be recognizable in as little as 1-2 years.

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Preferences & Distribution

Recorded distribution in Britain and IrelandRecorded in upper estuary cohesive mud in the Forth, Thames, Usk and Wye estuaries.

Habitat preferences

Depth Range
Water clarity preferences
Limiting Nutrients Field unresearched
Salinity
Physiographic
Biological Zone
Substratum
Tidal
Wave
Other preferences Cohesive mud; low interstitial salinity

Additional Information

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Species composition

Species found especially in this biotope

Rare or scarce species associated with this biotope

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Additional information

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Sensitivity reviewHow is sensitivity assessed?

Explanation

The cohesive muds of upper estuaries under tidal freshwater may be dominated by the oligochaete worms, Limnodrilus hoffmeisteri and Tubifex tubifex, besides being important characterizing species that are tolerant of very low interstitial salinity, they are primarily considered to be key functional species. They represent a major pathway for the transfer of energy from the sediment to secondary consumers (see productivity) and through their subsurface ingestion of organic matter and surface egestion, they regulate the depth of the anoxic layer to some extent, as biological and chemical oxidation proceeds more rapidly in oxygenated water at the surface than by anaerobic processes at depth (see ecological relationships). In their absence the cohesive mud of very low interstitial salinity, may become anoxic owing to bacterial degradation of the often considerable amount of organic matter within the sediment. A significant change in the infaunal community may occur.
Gammarid shrimps e.g. Gammarus zaddachi and Gammarus salinus are errant species that migrate into upper estuary tidal waters at certain times of the year, whilst they are not restricted to the biotope, their presence may affect the sensitivity of the biotope.

Species indicative of sensitivity

Community ImportanceSpecies nameCommon Name
Important otherGammarus spp.A gammarid shrimp
Key functionalLimnodrilus hoffmeisteriAn oligochaete
Key functionalTubifex tubifexAn oligochaete

Physical Pressures

 IntoleranceRecoverabilitySensitivitySpecies RichnessEvidence/Confidence
High High Moderate Major decline Moderate
Removal of the substratum would result in removal of the habitat and its associated community, therefore an intolerance of high has been recorded. Recovery will depend on recruitment from similar habitats. Although oligochaetes, Limnodrilus hoffmeisteri and Tubifex tubifex are common species, development of their juveniles is direct without a dispersive larval stage. Therefore, a recoverability of high has been recorded as it may take several years for the species to attain previous abundances, although in terms of species present the biotope may be recognizable in less.
Low Immediate Not sensitive Minor decline Low
Oligochaetes that characterize the biotope are infaunal with an ability to burrow through cohesive muds. They are unlikely to be adversely affected by an additional 5 cm covering of sediment. Gammarus species live in a variety of locations within the estuarine environment: amongst algae and other vegetation, as well as generally over the sediment surface and beneath stones. They are mobile species capable of a rapid escape response (back flip) if disturbed, however in the event of suddenly being smothered by 5 cm of sediment individuals resting on the surface may be killed, particularly so if the materials are viscous or impermeable. At the benchmark level an intolerance assessment of low has been made as key dominant species are unlikely to be killed, but the viability of gammarid species may be affected. Recoverability of the key functional oligochaete species has been assessed to be immediate as they will bury though additional sediment. However, effects on the whole community are likely to be more severe of smothering materials are viscous or impermeable.
Tolerant* Not relevant Not sensitive* No change Low
In the estuarine environment, fluctuations in the concentration of suspended sediment are to be expected e.g. owing to variation in surface runoff following precipitation, and may be measurable in grams per litre (benchmark is mg per litre). Oligochaete species characteristic of the biotope are unlikely to be adversely affected by elevated levels of suspended sediment as they are sub-surface deposit feeders. They may indirectly benefit from elevated levels of suspended sediment which may settle to the substratum where it may be utilized as a food resource. An assessment of not sensitive* has been made.
Low Not relevant No change High
The community is unlikely to be directly affected by a decrease in suspended sediment. However, such material may settle to the sediment where it is a utilisable food resource by the deposit feeding oligochaetes. Reduced levels of suspended sediment may therefore mean that the infaunal community experiences a reduction in food supply. An intolerance assessment of low has been made to reflect the likely impact on species viability in the long term. However, oligochaete species may also be especially abundant in less productive environments so on return to prior conditions optimal feeding is likely to resume and recovery has been assessed to be immediate.
Intermediate Very high Low Decline Low
The biotope is typically found in the infralittoral that is continually emersed, except for intermittent exposure of the sublittoral fringe on spring tides. The infaunal community of oligochaetes do not normally experience desiccation, so may be intolerant (especially juveniles) to continual exposure to sunshine and air for one hour as they are reliant on overlying water and their position in the substratum for protection. An assessment of intermediate has been made as desiccation stress may cause the death of some individuals. If a proportion of the oligochaete population capable of reproduction recovered, it is likely that recovery of the population to its previous abundance would be rapid following recruitment. Recovery has been assessed to be very high.
Low Very high Very Low Minor decline Low
The biotope is typically found in the infralittoral that is continually emersed, except for intermittent exposure of the sublittoral fringe on spring tides. Increased emergence of the sublittoral fringe may mean that the abundance of the oligochaete population in marginal areas may decrease, but significant changes in the community composition are unlikely and an assessment of low has been made. On return to prior conditions, the species are likely to repopulate marginal areas relatively rapidly through juvenile recruitment and adult migration. Recoverability has been assessed to be very high.
Tolerant* Not sensitive No change Moderate
The biotope is typically found in the infralittoral that is continually emersed, except for intermittent exposure of the sublittoral fringe on spring tides. A decrease in the emergence regime may be beneficial to the oligochaete population as additional habitat not subjected to desiccation would become available for colonization, and the physical extent of the biotope may increase. An assessment of not sensitive* has been made.
Intermediate High Low Decline Low
Locations where the biotope has been recorded typically experience very weak to weak tidal flow, which allows the deposition of fine sediments that characterize the biotope. Therefore, it is likely that with increased tidal flow, deposition of material would be impeded and deposits may be carried away, resulting in reduction of the available habitat. The effects of increased tidal flow may also be exacerbated by the infauna themselves. For instance, the bioturbatory activity of tubificids affects the stability of surface layers of sediment, as they loosen the sediment and render the surface layers susceptible to scour. When sediment scour occurs, under conditions of increased water flow, fine sediment particles and organic matter are carried into suspension and a high oxygen demand is created (HMSO, 1964; Edwards & Rolley, 1965). Gammarid species present in the biotope would probably experience difficulty in maintaining a position and be washed from the biotope. Whilst the oligochaete population is unlikely to be physically displaced from the cohesive mud, they may be affected by changes in the oxygenation of their habitat (see oxygenation, below) and by habitat loss. At the benchmark level an intolerance assessment of intermediate has been made in consideration of potential loss of habitat over the long term. On return to prior conditions, increased deposition of particulate matter would occur and habitat loss mitigated within a period of several years. Recoverability has been assessed to be high.
Tolerant Not sensitive* Not relevant
Locations where the biotope has been recorded typically experience very weak to weak tidal flow, which allows the deposition of fine sediments that characterize the biotope, so the community is unlikely to be directly adversely affected by reduced flow. At the benchmark level an assessment of not sensitive has been made for reduced water flow. However, reduced water flow may mean that water overlying the biotope begins to stagnate owing to reduced oxygen exchange and rapid utilization (the biotope has a high oxygen demand). The effects of reduced oxygen have been assessed separately (see oxygenation below).
Low Very high Very Low Minor decline High
Palmer (1968) (cited in Birtwell & Arthur, 1980) recorded large populations of Limnodrilus hoffmeisteri and Tubifex tubifex (up to 5.7 x 106m²) close to the heated effluent discharge of an electrical generating plant upstream of London Bridge on the River Thames. Birtwell & Arthur (1980) examined the tolerance of Tubifex tubifex from the Thames estuary to elevated temperature and found the 96 h LC50 value to be 33.9 °C, a temperature that would not be encountered within the main body of the estuary, but possible close to discharges of heated cooling water from electrical generating plants. In the same study, the tolerance of Limnodrilus hoffmeisteri was found to be even greater, its 96 h LC50 was 37.5°C. Although, evidently tolerant of elevated temperature, sub-lethal effects have been reported. For instance, Chapman et al. (1982) observed that at 10°C both Limnodrilus hoffmeisteri and Tubifex tubifex were capable of regulating their respiration, whilst at 20°C respiration rate was greatly elevated and only partially regulated. High temperatures have been reported to cause mortality of cocoons and will delay, but not prevent maturation of juveniles (see recruitment processes). Specimens of Gammarus salinus were tolerant of temperature fluctuations between 8 °C and 20 °C over a period of up to four weeks, acute temperature changes caused additional stress but did not result in mortality (Furch, 1972), as gammarid shrimps are very mobile they are able to avoid adverse conditions. At the benchmark level intolerance has been assessed to be low owing to Sub-lethal effects that may affect the recruitment of oligochaetes. Community composition is unlikely to significantly change and recoverability has been assessed to be very high.
Low Very high Moderate No change Low
The distribution of species within the biotope extends to locations north of the British Isles, so the community is likely to be tolerant of a chronic decrease in temperature of 2°C. Low water temperatures (< 10°C) were reported by Poddubnaya (1980) to cause significant levels of mortality in embryonic stages (within cocoon) of both Tubifex tubifex and Limnodrilus hoffmeisteri, and also delayed attainment of maturity, but did not prevent it. Intolerance to acute decreases in water temperature has been assessed to be low in consideration of effects upon recruitment of key functional species. Recoverability has been assessed to be very high, as recruitment by older individuals is not prevented.
Tolerant Not relevant Not relevant No change High
The light attenuating effects of an increase in turbidity are unlikely to affect a community dependent upon detrital organic matter for its productivity. An assessment of not sensitive has been made.
Tolerant Not sensitive* No change High
Changes in light penetration of the water column as a result of decreased turbidity are unlikely to affect a community dependent upon detrital organic matter for its productivity. An assessment of not sensitive has been made.
High High Moderate Decline Low
The biotope occurs in 'very sheltered' and 'extremely sheltered' areas (Connor et al., 1997a). This suggests that the biotope would be intolerant of wave exposure to some degree. An increase in wave exposure by two categories for one year would be likely to affect the biotope in several ways. Fine sediments would be eroded (Hiscock, 1983) resulting in the likely reduction of the habitat of the infaunal species, and a decreased supply of organic matter for deposit feeders which dominate the biotope. Oligochaetes buried at shallow depths may even be displaced and washed away, e.g. newly hatched juveniles. An intolerance assessment of high has been made, as through loss of muddy sediment, organic matter and new recruits the faunal composition of the biotope and physical habitat would change. On return to prior conditions, it may take several years for sufficient deposits of mud and organic matter to accumulate able to support the abundance of oligochaetes previously found. Recoverability has been assessed to be high. Although in terms of species present, the biotope may be recognizable in less time.
Tolerant Not sensitive* Not relevant
The biotope typically occurs in 'very' to 'extremely wave sheltered' locations (Connor et al., 1997a), and a decrease in wave exposure is unlikely to adversely affect the biotope. An assessment of not sensitive has been made.
Tolerant* Not relevant Not sensitive* No change Moderate
Infaunal oligochaetes may be able to detect vibration caused by localized noise and withdraw into the sediment, but are unlikely to be adversely affected by noise at the benchmark level. An assessment of not sensitive* has been made as birds that predate upon aquatic oligochaetes may temporarily be scared off.
Tolerant Not relevant Not relevant No change Moderate
Characterizing species are unlikely to possess the visual acuity to detect the visual presence of objects outlined in the benchmark. An assessment of not sensitive has been made.
Intermediate Very high Low Minor decline Low
In normal circumstances, the oligochaete community is on the whole protected from abrasion owing to their infaunal position, whilst gammarid species are able to rapidly move away from such disturbance. However, any object penetrating and dragging into the cohesive mud may cause displacement and damage to some individuals. Intolerance has been assessed to be intermediate. A proportion of the population capable of reproduction is likely to remain and recovery be rapid following a period of reproduction. Recoverability has been assessed to be very high
Tolerant Immediate Not relevant No change Moderate
Oligochaete and gammarid species found within the biotope are not permanently attached to the substratum. If displaced from a particular location the oligochaetes would probably be able to rapidly reburrow into the sediment, whilst gammarids are able to swim and crawl along the bottom to attain a favourable position. An assessment of not sensitive has been made. Recoverability has been assessed to be immediate.

Chemical Pressures

 IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
High High Moderate Decline Moderate
Oligochaetes may be especially susceptible to synthetic chemicals that bind to sediments. Evidence suggests that some synthetic chemicals would adversely affect the important functional species of oligochaetes in this biotope, through both lethal and sub lethal effects. For example, Lotufo & Fleeger (1996) investigated acute and sub-lethal toxicity of sediment spiked with pyrene and phenanthrene to Limnodrilus hoffmeisteri. Phenanthrene was acutely toxic at high sediment concentrations (297. 5 µg/g 10-day median lethal concentration), whilst pyrene was not acutely toxic, even at concentrations as high as 841 µg/g. Both chemicals adversely affected the feeding activity of Limnodrilus hoffmeisteri and some burrowing avoidance was detected in sediment spiked with high phenanthrene concentrations (143-612 µg/ g), but was not detected with pyrene. Offspring production was also significantly reduced in contaminated sediments.
  • Keilty et al., (1988) observed that endrin contaminated sediments inhibited the burial of Limnodrilus hoffmeisteri. Dad et al., (1982) reported on the acute toxicity and presumable harmless concentration of two commercial insecticides, Furadan 3G and Matalaf 50 E, for Limnodrilus hoffmeisteri and Tubifex tubifex. Limnodrilus hoffmeisteri was found more susceptible to both insecticides, with Furadan being the most toxic. Sub-lethal effects including reduced reproductive potential have been reported for gammarid species exposed to a surfactant TWEEN 80 and pentachlorophenol (PCP) and benzo[a]pyrene (B[a]P) (Lyes, 1979; Lawrence & Poulter, 2001).
    intolerance has been assessed to be high as species within the biotope may decline in abundance. Recovery will depend on recruitment from survivors within and from similar habitats. Although oligochaetes, Limnodrilus hoffmeisteri and Tubifex tubifex are common species, development of their juveniles is direct without a dispersive larval stage. Therefore, a recoverability of high has been recorded as it may take several years for the species to attain previous abundances, although in terms of species present the biotope may be recognizable in less.
  • Heavy metal contamination
    Low High Low Minor decline Moderate
    Heavy metal studies with oligochaetes have concentrated almost exclusively on tubificids, in particular Limnodrilus hoffmeisteri and Tubifex tubifex . Chapman et al., (1980) reviewed the literature available on the subject and concluded both species to be particularly tolerant of heavy metal contamination. Early work concentrated on determining LD50 concentrations and ranking toxicity, e.g. Brkovic-Popovic & Popovic (1977) suggested that tubificid oligochaetes were most intolerant of Cu, Cd and Hg in solution than to Zn, Cr, Ni and Pb. However, as tubificids are infaunal species that are not directly exposed to conditions in the water column, their tolerances to heavy metals should be considered on the basis of metal levels in sediments and interstitial water. Wensel et al. (1977) measured metal levels in Palestine Lake, Indiana by nitric-perchloric digestion and found that Limnodrilus spp. survived Cd, Zn and Cr levels (in µg/g dry weight) of 970, 14000 and 2100 respectively. These levels had eliminated most of the rest of the benthos.
    The emphasis of more recent research has moved to the detection of sub-lethal effects as a more sensitive indicator of toxicity. Reported sub-lethal effects of certain metals on Limnodrilus hoffmeisteri and Tubifex tubifex include reduced and elevated respiration rates, decreased concentration of haemoglobin, autotomy, excessive mucus production and reduced number of cocoons arising from reproduction (Whitley & Sikora, 1970; Brkovic-Popovic & Popovic, 1977b; Vecchi et al., 1999; Martinez-Tabche et al., 1999; Bouche et al., 2000). Research has also focused on the mechanisms of oligochaete resistance to metal toxicity. Klerks & Levinton (1989) reported that Limnodrilus hoffmeisteri from a metal polluted cove had evolved resistance to a combination of Cd, Ni and Co and Klerks & Bartholomew (1991) examined the physiological mechanisms by which such resistance is achieved. A later paper by Martinez & Levinton (1996) suggest that one gene controls resistance to metal in the metal tolerant aquatic oligochaete Limnodrilus hoffmeisteri.
    an intolerance assessment of low has been made in order to indicate that the aquatic oligochaetes of this biotope are especially tolerant of certain heavy metals, but that sub-lethal effects occur. Reports of mass mortalities of these particular tubificids in the natural environment were not found, so it is likely that owing to the ability for resistance to evolve within a population specimens will survive and recovery of the community is likely.
    Hydrocarbon contamination
    Intermediate Very high Low Decline Moderate
    Little information is available specifically concerning the effects of hydrocarbon contamination on oligochaete populations. The IMU.LimTtub biotope occurs in low energy environments protected from wave and tidal flow in upper estuaries. Sediments are rich in organic matter, and in the event of an oil spill, the high organic content promotes sorption of oil into the sediments. Furthermore, in such environments the bacterial degradation of oil is hindered by conditions of low oxygenation. The best documented oil spill in a protected habitat with soft mud/sandy substrata is the 1969 West Falmouth spill of #2 diesel fuel (Sanders, 1978). As a consequence of conditions outlined above, remobilisation of oil (especially within subtidal regions) continued for more than a year after the original spill and caused greater contamination than the initial impact. Virtually the entire fauna was eradicated following the spill, but populations of opportunistic species soon flourished. In the case of the West Falmouth spill, Capitella capitata reached a population abundance >200, 000 m² (Sanders, 1978). Capitella capitata will tolerate 'variable' salinity and is absent in low salinity regions of upper estuaries, instead the aquatic oligochaetes capable of rapid reproduction are likely to flourish. For instance, following the Exxon Valdez spill in Prince William Sound, Alaska, the abundance of oligochaetes in the intertidal region was noted to have increased, and more than 10 years after the spill their continued presence may be indicative of a subtle but significant alteration in the infauna of Prince William Sound (Highsmith et al., 1996; McRoy, 2000). Although, the infauna may be eradicated in the worst affected areas, e.g. through direct effects of toxicity, smothering and deoxygenation (sensitivity assessed elsewhere), fringe populations of oligochaetes in less affected areas may benefit primarily from the additional food resources (bacteria & micro-organisms) that arise, and are likely to transfer ingested contaminants from the sediment directly to other food web predators, e.g. birds, fish and predatory invertebrates.
    On balance, intolerance to hydrocarbon pollution has been assessed to be intermediate. A proportion of the oligochaete population may killed in the worst affected areas, whilst in the longer term, fringe populations may benefit and increase in abundance. Owing to the life cycle of the aquatic oligochaetes characteristic of this biotope, recovery is likely to be rapid and defaunated areas recolonized. Recoverability has been assessed to be very high.
    Radionuclide contamination
    No information Not relevant No information Not relevant Not relevant
    Insufficient
    information.
    Changes in nutrient levels
    Tolerant* Not relevant Not sensitive* No change High
    The aquatic oligochaetes, Limnodrilus hoffmeisteri and Tubifex tubifex, are characteristic and key functional species of this biotope. They are subsurface deposit feeders, that thrive in the organically enriched sediments of many upper estuarine environments, an environment which has historically received organically enriched effluents from sewerage treatment and industry. These species will respond positively with increased abundance to organic enrichment (except in abiotic zones), as it is an important food resource. McLusky et al. (1980) and Birtwell & Arthur (1980) give accounts of the effects of organic enrichment on the abundance and community composition of oligochaetes in the Forth estuary, Scotland and Thames estuary, S. England, resulting from organic enrichment in combination with environmental parameters.
    At the benchmark level, an assessment of not sensitive* has been made, as the abundance of species characteristic of the biotope is likely to increase.
    High High Moderate Rise High
    Interstitial salinity is an important factor determining the occurrence of the IMU.LimTtub community. The key functional species, Limnodrilus hoffmeisteri and Tubifex tubifex, are essentially freshwater species, able to tolerate very low interstitial salinities and therefore able to penetrate from freshwater ecosystems into upper estuaries, which although tidal, are dominated by freshwater conditions, e.g. the upper Forth estuary, Scotland (see McLusky et al., 1980). As salinity increases seawards, the infaunal species composition and indeed the dominant class of annelid eventually changes, so that larger estuarine polychaetes become important bioturbators (Diaz, 1980).
    Stczynska-Jurewicz (1972) reported that the maximum salinity at which Tubifex tubifex could survive was 9 psu and the maximum at which natural egg laying and development occurred was 4 psu. Kennedy (1965) stated that salinity also controlled the distribution of Limnodrilus hoffmeisteri, but gave no precise limits. In the Forth estuary, McLusky et al. (1981) found Tubifex tubifex in localities with a maximum salinity of 4.1 psu, and Limnodrilus hoffmeisteri occurred at salinities of up to 7.7 psu, these species dominated the initial 16 km of the estuary from Stirling. Between 16 and 28 km the interstitial salinity increased progressively from a mean of 3.2 psu to 26.4 psu, and over that stretch of the estuary the dominant oligochaete was Tubifex costatus. Tubificoides benedeni (as Peloscolex benedeni) became the dominant oligochaete in the lower part of the estuary. This estuarine succession of Tubifex tubifex and Limnodrilus hoffmeisteri, then Tubifex costatus, then Tubificoides benedeni, was also found by Hunter and Arthur (1978) in the Thames estuary. This evidence suggests that the IMU.LimTtub biotope would be highly intolerant of increased salinity and that community composition of the infaunal oligochaete community would change. Intolerance has been assessed to be high. On return to prior conditions, recovery would probably br high as species distribution and abundance would again correlate to limits of salinity tolerance.
    Tolerant Not sensitive* No change High
    The key functional oligochaete species, Limnodrilus hoffmeisteri and Tubifex tubifex, are freshwater aquatic oligochaetes, able to penetrate from freshwater ecosystems into upper estuaries, which although tidal, are dominated by freshwater conditions, e.g. the upper Forth estuary, Scotland (see McLusky et al., 1980). Typical salinities recorded for the biotope are 'low' (< 18 psu) (Connor et al., 1997a), the benchmark decrease in salinity would mean that the community would be exposed to freshwater. Limnodrilus hoffmeisteri and Tubifex tubifex are not likely to be adversely affected. To a certain extent the distribution of Gammarus species is also correlated with salinity. Distinct zonation patterns may be observed, Gammarus salinus prefers intermediate salinities, whilst Gammarus zaddachi and Gammarus duebeni predominantly live in more dilute brackish waters, locally penetrating into freshwater transition zones (Bulnheim, 1984). At the benchmark level, a decrease in salinity is unlikely to cause significant changes in community composition, and an assessment of not sensitive has been made.
    Low Very high Very Low No change High
    Research by Birtwell & Arthur (1980) on the ecology of tubificids in the Thames estuary included investigation of their tolerance of anaerobic conditions and low dissolved oxygen concentrations in the field.
    In laboratory studies, Limnodrilus hoffmeisteri was found to have a greater anaerobic tolerance than Tubifex tubifex at all water temperatures tested (20, 25 & 30°C). At 20°C, Limnodrilus hoffmeisteri had a LC50 time of 52 h, whilst Tubifex tubifex had a LC50 time of 28 h. At 30°C the LC50 for Limnodrilus hoffmeisteri decreased to 18 h, Tubifex tubifex also had a decreased tolerance at 30°C with a LC50 of 12 h. In the field, populations of the two species seemed able to tolerate conditions of low dissolved oxygen and periodic episodes of < 5% air saturation (< 2 mg O2 L). For example, large populations of Limnodrilus hoffmeisteri occurred on the Thames between Greenwich and Woolwich, where average weekly dissolved oxygen concentration was just 2 mg/O2/L between December 1968 and September 1971 (see Table 2. in Birtwell & Arthur, 1980) and frequently dropped below this level. Birtwell & Arthur (1980) suggested that the low metabolic rate of Limnodrilus hoffmeisteri, coupled with its relatively better ability to survive periodic anaerobic conditions without incurring an oxygen debt, suited its survival in such locations. Although, Tubifex tubifex demonstrated a relatively lower tolerance to anaerobic conditions than Limnodrilus hoffmeisteri, it occurred in locations with a low average oxygen concentrations and survived periodic anoxia, although such situations were considered by Birtwell & Arthur (1980) to be less conducive to the establishment of populations of Tubifex tubifex.
    Embryos of both species are intolerant of low oxygen concentrations in combination with low temperature (see recruitment processes). Fisher & Beeton (1975) noted from vertical burrowing experiments in conditions of anoxia, that a more even distribution of Limnodrilus hoffmeisteri occurred in the upper 6 cm of sediment than in controls, and in vertical burrowing experiments avoidance of anoxic sediment was significant.
    At the benchmark level, intolerance of the key functional oligochaetes has been assessed to be low, as populations are likely to persist in conditions of a low dissolved oxygen concentration for a week, although such conditions maybe less conducive to the recruitment of juveniles. Should anaerobic conditions be experienced for a period of a week mortalities would be expected.

    Biological Pressures

     IntoleranceRecoverabilitySensitivityRichnessEvidence/Confidence
    No information Not relevant No information Not relevant Not relevant
    Limnodrilus hoffmeisteri is parasitized by the caryophyllidean cestode Archigetes iowensis (Williams, 1979). Tubifex tubifex is an intermediate host to a myosporean parasite, Myxobolus macrocapsularis (Myxosporea: Myxobolidae) of the common bream, Abramis brama (Szekely et al., 2002). Tubifex tubifex is also an intermediate host to the parasite Myxobolus cerebralis which causes Salmonid Whirling Disease (Zendt & Bergersen, 2000). However an assessment of insufficient information has been made as no information concerning effects on the population was found.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    No non-native species are known to adversely impact upon the biotope. An assessment of not relevant has been made.
    Not relevant Not relevant Not relevant Not relevant Not relevant
    It is extremely unlikely that any of the species indicative of sensitivity would be targeted for extraction and we have no evidence for the indirect effects of extraction of other species on this biotope.
    Not relevant Not relevant Not relevant Not relevant Not relevant

    Additional information

    No text entered

    Importance review

    Policy/Legislation

    Habitats Directive Annex 1Estuaries

    Exploitation

    No text entered.

    Additional information

    -

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    Citation

    This review can be cited as:

    Budd, G.C. 2002. Limnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment. In Tyler-Walters H. and Hiscock K. (eds) Marine Life Information Network: Biology and Sensitivity Key Information Reviews, [on-line]. Plymouth: Marine Biological Association of the United Kingdom. Available from: http://www.marlin.ac.uk/habitat/detail/35

    Last Updated: 01/11/2002