Limnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment
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 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.
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.
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).
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.
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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This review can be cited as follows:
Limnodrilus hoffmeisteri, Tubifex tubifex and Gammarus spp. in low salinity infralittoral muddy sediment.
Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on-line].
Plymouth: Marine Biological Association of the United Kingdom.
Available from: <http://www.marlin.ac.uk/habitatecology.php?habitatid=35&code=2004>