A comparison of two tubificid oligochaete species as candidates for sublethal bioassay tests relevant to subtropical and tropical regions

Two tubificid oligochaetes, Branchiura sowerbyi and Tubifex tubifex, were evaluated as potential test organisms for sediment bioassays. We attempt to reproduce the sediment bioassay proposed by Reynoldson et al. (1991) using his strain of Tubifex tubifex and his reference sediment and to compare this technique using Branchiura sowerbyi. This species was chosen because it is more common and dominant in tropical and subtropical environments than Tubifex tubifex. Data on survival and reproduction were obtained for both species, and growth estimates were obtained for B. sowerbyi. The sublethal bioassay with T. tubifex confirmed earlier estimates of a test duration of 4 weeks at 22.5 °C. B. sowerbyi cultures can produce usable estimates in 21 days at 30 °C.     

The bottom Oligochaeta communities in sand pits of different trophic status in Upper Silesia (Southern Poland)

Oligochaeta, occurring in the littoral zones of two sand pits, were sampled in order to determine the relationship between the oligochaete species and the waters’ trophic level. Differences between sand pits attributable to community structure and to an overall higher abundance of oligochaetes, especially tubificids, were observed in Dzierżno Małe. Multivariate analyses (correspondence analysis [CA] and canonical correspondence analysis [CCA]) reveal correlations between the distribution patterns of oligochaete species and the concentration of nitrates, phosphates and dissolved oxygen. Some species, e.g. Dero digitata, Limnodrilus hoffmeisteri, Potamothrix hammoniensis, Nais simplex, Limnodrilus claparedeanus, Limnodrilus udekemianus and Tubifex tubifex, were more abundant in eutrophic sites. The results of the study showed that the richness of Oligochaeta species is not a good method for estimating the trophic levels of the studied sand pits. Indicators based on the share of oligo-, meso- and eutrophic species in Oligochaeta communities are better for evaluating the water quality in the studied reservoirs.     

A morphological reappraisal of Tubifex blanchardi Vejdovský, 1891 (Clitellata: Tubificidae)

Tubifex blanchardi Vejdovský, 1891 is a freshwater tubificid, often living in sympatry with Tubifex tubifex (Müller 1774). Although considered from its discovery as a species on its own, its biological status is debated. During the early seventies T. blanchardi was reduced to a mere form of T. tubifex, as a particular case of polymorphism in chaetal pattern. Using classical histological techniques, microdissections of portions of the male genital apparatus and phalloidin staining of dissected copulatory organs we investigated 163 mixed individuals of T. blanchardi and T. tubifex belonging to sympatric populations from the Lambro River (Milan, Northern Italy). The internal morphology of T. blanchardi is described for the first time. Our results show that T. tubifex and T. blanchardi differ in several characters concerning both their external and internal morphology, and in the fine organization of their copulatory organs. Several independent character sets support the separation of T. blanchardi from T. tubifex, suggesting that it is an independent species. This study also supports the idea that T. blanchardi and T. bergi (Hrabě, 1935), another species closely related to T. tubifex, are not conspecific. The observed morphological differences between allopatric populations of T. tubifex are discussed.     

Expression pattern of annelid <Emphasis Type="Italic">Zic</Emphasis> in embryonic development of the oligochaete <Emphasis Type="Italic">Tubifex tubifex</Emphasis>

Embryonic expression of a Zic homologue (Ttu-Zic) was examined in the oligochaete annelid Tubifex tubifex. The body plan of T. tubifex is characterized by obvious segmentation in the ectoderm and mesoderm. Ttu-Zic expression is detected in the mesodermal germ band and a subset of micromere descendants. Ttu-Zic is transiently expressed in primary m-blast cells (i.e., founder cells of mesodermal segments) as early as the time of their birth from M teloblasts. During its development, each mesodermal segment experiences two additional phases of Ttu-Zic expression. Ttu-Zic expression in micromere descendants is seen on the anterior surfaces of embryos undergoing teloblastogenesis; subsequently, these cells proliferate to form bilateral clusters, which then become internalized. Finally, clusters of Ttu-Zic-expressing cells are found in the center of the prostomium, corresponding to the cerebral ganglion. The Ttu-Zic expression profile in the early embryogenesis of T. tubifex may be homologous to those of evolutionarily distant animals.     

Observations on cohorts of Tubifex tubifex cultured at different food levels,using cellulose substrate

In order to clarify the relationship between food availability and population dynamics in aquatic oligochaetes, short term cultures and cohort cultures of Tubifex tubifex were reared using substrates with different food concentrations, obtained by mixing sand with different amounts of cellulose powder.In short term experiments, T. tubifex seemed capable of utilizing cellulose substrates for growth or egg production. Yet, in the cohort experiment, newly hatched worms could not grow on cellulose substrates. Survivorship, however, appears to be influenced by cellulose concentration giving an indication that this material, although inadequate, is somehow utilized.     

Composition and distribution of bottom oligochaete fauna of a north Italian eutrophic lake (Lake Ledro)

The profundal macroinvertebrates, particularly the oligochaetes, of Lake Ledro (Trento, Italy), that has recently undergone eutrophication, were studied.A statistical approach of random sampling was used to study the distribution and abundance of the oligochaete species. The optimum sample number was calculated from a preliminary sample series. The oligochaete community was made up of five tubificid species, one naidid and one lumbriculid species that on average represents more than 80% of the macrobenthic community. Population density was correlated with depth and decreasing oxygen concentration. The role of Tubifex tubifex as a eutrophic, tolerant species was confirmed; and in fact it was the only species found (although at low density) in the deepest and anoxic zone. No comparable data are available for the lake prior to eutrophication, but these data will be valuable for future comparison once a remediation program for the lake has been implemented.     

Some aquatic oligochaetes of the Nilgiris,South India

Eight species of aquatic oligochaetes, belonging to the families Naididae and Tubificidae, are reported, of which six species are new to the Nigiris. Tubifex tubifex known from Coonoor is reported again from this area.     

Disappearance of deep profundal zoobenthos in Lake Ikeda, southern Kyushu, Japan, with relation to recent environmental changes in the lake

A benthological survey in a deep caldera, Lake Ikeda, southern Kyushu, Japan, in 1998 revealed that no zoobenthos were found in the deep profundal, although two tubificid oligochaetes, Tubifex tubifex and Limnodrilus hoffmeisteri, and a chironomid, Procladius sp., were distributed in the upper profundal zone. This is the first record of oligochaete composition in the lake. Lake Ikeda had been typically oligotrophic until the 1940s, and zoobenthic assemblages were recorded throughout the profundal bottom in the 1920s and 1970s. Recent disappearance of the deep profundal zoobenthos could be caused by the stagnation of anoxic waters in the hypolimnion, in connection with eutrophication triggered by nutrient loading, as well as change in the thermal circulation system presumably caused by global warming.     

Meiofauna of the profundal zone of the northern part of Lake Ladoga as an indicator of pollution

Benthic meiofauna was sampled at 19 stations, mainly in the northern part of Lake Ladoga, from depths between 13 and 199 m and from types of environment ranging from sheltered areas near pollution sources to less polluted open areas. About 80 taxa were identified, of these 70 to the species level. The greatest numbers of species were oligochaetes (24 species) and harpacticoids (8 species). Certain quantitative ratios of meiofauna were shown to be correlated with environmental data. The species of the oligochaete families Lumbriculidae and Aeolosomatidae and the harpacticoids as a collective group, excluding Canthocamptus staphylinus, were most clearly confined to the less eutrophied environments. The oligochaete species Amphichaeta leydigii, Dero digitata and Tubifex tubifex, the resting stages of Cyclopinae, and Eucyclops serrulatus among the Eucyclopinae were most clearly concentrated in the eutrophicated or polluted environments. The groups of Naididae, Cladocera and Eucyclopinae did not have much value as indicators. Shannon diversity index correlated positively with the total phosphorus content of the water, and number of species decreased with increasing depth. In general, it seems that the pollution tolerance of the meiofauna in a very large lake such as Lake Ladoga is high, presumably due to the effective mixing of water masses.     

Host–parasite interactions and competition between tubificid species in a benthic community

1. Parasites can be important determinants of host community structure while host community structure can influence the success of parasites, although both are often overlooked. In two laboratory experiments, we examined interactions among Myxobolus cerebralis syn Myxosoma cerebralis Höfer, the myxozoan parasite that causes salmonid whirling disease, and two coexisting tubificid species: Tubifex tubifex (Müller), which is the alternate host of the parasite, and Limnodrilus hoffmeisteri Claparède, which is not susceptible. In the first experiment, we examined T. tubifex infection prevalence when exposed to nine doses of spores. In the second experiment, we examined tubificid and parasite success under three spore doses when tubificids were combined in a response surface experimental design used to detect interactions among species. 2. The outcomes of interactions between tubificid species were complex. The number and biomass of offspring of both tubificid species were density dependent when in monoculture or in combination with the other species. Adult growth of T. tubifex was also density dependent in monoculture, but when L. hoffmeisteri replaced one‐half of the T. tubifex in the high‐density treatment, adult growth of T. tubifex was higher than in monoculture. Adult growth of L. hoffmeisteri was always density independent. Whether T. tubifex was exposed to the parasite or not did not change the outcome of these interactions. However, adult growth of T. tubifex, but not L. hoffmeisteri, was highest when M. cerebralis was present. 3. Infection prevalence of T. tubifex increased with increasing spore dose. Infection prevalence was lowest in the high‐density T. tubifex monoculture and highest in the low‐density T. tubifex monoculture and when T. tubifex was in combination with L. hoffmeisteri. 4. Both intraspecific and interspecific competition influenced tubificid success, but T. tubifex gained some competitive advantage through increased adult growth when in combination with L. hoffmeisteri. Whether T. tubifex was exposed to the parasite or not did not change the outcome of the interactions between the tubificid species. 5. The presence of L. hoffmeisteri did not decrease the prevalence of infection in T. tubifex, suggesting that parasite success was unaltered by the presence of this non‐susceptible species.     

Tubifex tubifex as a link in food chain transfer of hexachlorobenzene from contaminated sediment to fish

Sediments contaminated with poorly water-soluble organic chemicals pose a risk to aquatic food chains. Sediment-associated chemicals can be accumulated by endobenthic, sediment-ingesting invertebrates. Some tubificid species – or other benthic annelids – serve as food for benthivorous fish, which thereby ingest the sediment-borne chemicals and may accumulate contaminant concentrations far higher than from water exposure only, and transfer them to organisms of higher trophic levels. For measurement of biomagnification, a sediment based food chain was developed and established in the laboratory. The two-step food chain included the sediment-dwelling freshwater oligochaete Tubifex tubifex (Müller) as a representative species of benthic infauna. The three-spined stickleback (Gasterosteus aculeatus, Linné), a small teleost fish which often feeds primarily on benthic invertebrates, served as a model predator. Spiked artificial sediment and reconstituted water as the overlying medium were used. Experiments were performed using ¹⁴C-labelled hexachlorobenzene, a hydrophobic pollutant as a model compound. To examine the influence of benthic prey on the bioaccumulation of the test substance in the predator, fish were exposed to spiked water, spiked sediment, pre-contaminated prey organisms, or combinations of these exposure routes. The results of these experiments indicate that for hexachlorobenzene, the presence of contaminated Tubifex tubifex as a food source in combined exposure leads to significantly higher accumulation in fish than exposure to single pathways.     

Molecular phylogeny of tubificid oligochaetes with special emphasis on Tubifex tubifex (Tubificidae)

Tubifex tubifex is a cosmopolitan freshwater oligochaete whose presence has been studied as a health indicator of the aquatic environment and as a host for several myxozoan parasites of fish. Unfortunately, current morphological criteria used to distinguish Tubifex spp. (Tubificidae) are inadequate. We therefore developed mitochondrial 16S ribosomal DNA markers to examine phylogenetic relationships among aquatic oligochaetes and to distinguish species of Tubifex that might serve as hosts for a particular myxozoan parasite, Myxobolus cerebralis. Our phylogenetic analyses of oligochaetes based on a 378-bp segment yielded one most parsimonious tree with three major groups that corresponded to the families Lumbricidae, Sparganophilidae, and Tubificidae. T. tubifex and T. ignotus formed a monophyletic assemblage, and a sister relationship between the genera Tubifex and Limnodrilus was strongly supported. A second analysis of the relationship within the genus Tubifex identified six genetically distinct lineages of T. tubifex from North America and Europe that were separated by genetic distances comparable to those found for "well-defined" species of Limnodrilus. Therefore, the existence of several morphologically indistinguishable, thus cryptic, species of Tubifex in North America and Europe is suggested.     

Inorganic carbon fluxes at the water–sediment interface in five littoral systems in Spain (southern Europe)

The assemblage of littoral oligochaetes in six crater lakes in Central Mexico, was studied throughout a yearly cycle. To establish species composition, richness, density and biomass, 14 localities were sampled in the lakes. A total of eight species belonging to the families Naididae (five species), Tubificidae (two species), and Enchytraeidae (one species) were found. The dominant species, Limnodrilus hoffmeisteri, contributed with up to 99% in both abundance and biomass. Sediment organic matter is the most important environmental variable explaining the differences in density and biomass. Seasonal (dry and rainy seasons) changes were not significant for density and biomass. Higher density and lower biomass values characterized these lakes in contrast to other tropical and subtropical lakes worldwide. The small size of the dominant species L. hoffmeisteri was recorded in all lakes and explained the low biomass recorded in the area of study. The correlation between L. hoffmeisteri and four other species (Dero (Dero) nivea, D. (D.) digitata, Nais variabilis and Tubifex tubifex) was negative. The naidid species were positively correlated (>0.5) to each other.     

The Influence of Environmental Factors and Microhabitat Availability on the Distribution of an Aquatic Oligochaete Assemblage in a Mediterranean River Basin

Some aquatic oligochaete species, mainly certain naidids and tubificids, are often associated with polluted environments, with high levels of organic matter and oxygen deficit. However, in the stations sampled in the Guadaira river basin, which can be arranged on an axis of organic pollution, the main aquatic oligochaete species (Nais elinguis and Tubifex tubifex) inhabiting these environments do not show a distribution pattern significantly related to the water physico-chemical characteristics measured. Nor, have we registered any association between these species and any kind of microhabitat, defined here: water current, presence of different types of vegetation, substrate coarseness and presence of anoxic sediments. Paranais litoralis is the exception, being related to areas without water current, located at higher altitudes, with high levels of dissolved organic matter and an anoxic substrate made up of fine particles. These results can be explained by the highly fluctuating nature of Mediterranean ecosystems and by the marked generalist character and ubiquity of the oligochaete assemblage species, able to colonize any kind of environment.     

Cyst formation of Tubifex tubifex (Müller) — an adaptation to survive food deficiency and drought

Adult individuals of Tubifex tubifex (Müller) (Oligochaeta, Tubificidae) could be induced to form cysts in the laboratory. Hiding in cysts, Tubifex tubifex survived a five-month drought period in the field. Encysted Tubifex tubifex had a lower super-cooling-point than mobile individuals. Food shortage is believed to be the main factor in cyst formation.     

Beyond Masses and Blooms: The Indicative Value of Oligochaetes

The European Water Framework Directive (WFD) defines a framework for assessing water bodies in Europe in the future. The conditions in the Directive impose a strong demand for “new” assessment systems. The AQEM project developed an assessment system for European streams using macroinvertebrates. Almost 900 samples were taken in about 400 streams covering 29 stream types distributed over eight countries. The role of the Oligochaeta within this European database was analysed. Almost half a million specimens of oligochaetes were collected in 772 samples. Eight families, 41 genera and 69 species were recorded, although identification emphasised the families Tubificidae and Naididae. Three countries identified oligochaetes to species level, most others restricted their identifications to easy identifiable taxa. Numbers of specimens, species, genera and families differed strongly between the countries due to method, although standardised, and taxonomic knowledge. About 50% of all collected oligochaete taxa had assigned biological and ecological indicator values for metric calculation in the AQEM assessment system. A further refinement of this indication list as well as increased coverage of oligochaete taxa was advised. Weighted averaging was used to evaluate the relation between oligochaete distribution and ecological quality class. It was concluded that when higher taxonomic levels are used in assessment, the quality evaluation results become biased. Furthermore, oligochaetes can tell us much more about the ecological status of streams than is commonly assumed. Differences in ecological optima among Limnodrilus udekemianus, Ilyodrilus templetoni, Aulodrilus pluriseta, Nais communis, and Spirosperma ferox are shown.     

Actinosporean infections in oligochaetes in a river system in southwest Ireland with descriptions of three new forms

Sediment samples were collected in April, June and August 1998 from a river in southwest Ireland. A total of 1,836 oligochaete specimens were collected from these sediments, and examined for actinosporean infections. Actinosporean-infected oligochaetes have been determined, symptoms and course of infection have been considered and the spores released from them have been described. Spore characteristics for each actinosporean were defined and the prevalence of infection in each oligochaete species was also determined. The overall prevalence of infection with actinosporeans within the oligochaete sample was approximately 2%. Seven types were distinguished, belonging to echinactinomyxon, aurantiactinomyxon and neoactinomyxum forms, from Tubifex ignotus, Lumbriculus variegatus and Limnodrilus hoffmeisteri, and compared with actinosporean types previously reported in the literature. Three of these forms have not been previously described, while the other 4 are morphologically and morphometrically similar to known forms. These actinosporeans may be stages in myxozoan life cycles.     

Indicative profundal oligochaete assemblages in selected small Swedish lakes

Fifty-seven small- to middle-size lakes of Sweden (size-range from <0.1 to about 200 km²) representing different regions and lake-types were selected for the purpose of demonstrating the indicative value of profundal oligochaete communities also of relatively small lakes. It is well known since previously that profundal oligochaete assemblages of large lakes in Europe may be particularly indicative of the current trophic situation, but little has been known about smaller lakes in this respect. Characterizations based on oligochaete community structure in these lakes could be summarized in eight different groups: Characteristic oligochaete communities in oligotrophic lakes of relatively small size are Spirosperma ferox, Stylodrilus heringianus and Tubifex tubifex. Oligochaete species richness is low (1–3 species) and so is species abundance (<300 specimens m^–2). Very eutrophic lakes of the same size-range are largely dominated by the tubificids Limnodrilus hoffmeisteri and/or Potamothrix hammoniensis. Substitute or complementary species may be T. tubifex. Species richness is usually low (1–3 species), but abundance is high to very high (>5000 specimens m^–2). Mesotrophic to moderately eutrophic lakes of the same size categories contain more species than the above extremes, most of them being fairly tolerant to oxygene deficiency such as Tubifex ignotus, a number of species of the genera Aulodrilus and Limnodrilus and a variety of so-called Ponto-Caspian Potamothrix species, most of them having recently invaded south-eastern Sweden. Species richness is moderate to high (4–8 species), while abundance may vary considerably (range from about 300 to about 5000 specimens m^–2). In this respect, small- to middle-size lakes do not differ much from larger lakes. For the trophic characterization of lake water the mean concentrations of total-phosphorus (in g l^–1) is generally regarded to be the most appropriate measure. The match between characterizations based upon oligochaete community structure and total-phosphorus concentrations is generally very good for large lakes. The present study shows that this applies fairly well also to the majority of the small- to middle-size lakes selected for this study. This has not been shown before. Obvious deviations from this rule could be caused by a scarcity of reliable chemical data, or considerable seasonal shifts in the chemical composition ot the water, which in its turn may be caused by short water residence time. Littoral elements in the fauna, which are generally less indicative, or effects of local inflows may also be more frequent here than in lakes of larger size.     

An ultrastructural overview of tubificid spermatozoa

The spermatozoa of seven species of tubificid oligochaete were compared to those already described in order to supply spermatozoal characters for systematic work on Tubificidae. The spermatozoa of Clitellio arenarius (subfamily Tubificinae) resemble those of the two other known members of the subfamily (Tubifex tubifex and Tubificoides amplivasatus) in being of two different types and in showing the same morphology of acrosomes and nuclei. Among Phallodrilinae, the three gutless species Inanidrilus bulbosus, Inanidrilus leukodermatus and Olavius planus share with Bathydrilus formosus the shape of the nucleus and various characters of the acrosome, whereas Thalassodrilus prostatus is particular in having the acrosome vesicle external to the tube and the longest middle piece recorded in oligochaetes. Monopylephorus limosus and Rhizodrilus russus (Rhyacodrilinae) differ widely in acrosomal and nuclear characters: M. limosus has a twisted nucleus, whereas R. russus has an apically flanged nucleus with a conspicuous apical concavity and an endonuclear canal. The data published on spermatozoa of the Limnodriloidinae are reviewed.Department of Zoology University of Göteborg