A Comparative Structural Study on Bacterial Symbioses of Caribbean Gutless Tubificidae (Annelida,Oligochaeta)

The bacterial symbiosis in 13 different species of the gutless phallodriline genera Inanidrilus and Olavius (Tubificidae, Oligochaeta) from Carrie Bow Cay (Belize), Florida and Bermuda is structurally compared. The result is an essentially consistent symbiotic pattern regarding the position and ultrastructural design of the prokaryotic partners and their integration in the anatomy of the animal hosts. Based on numerous micrographs, it is calculated that the endobacteria comprise about 25% of the host's volume. This corresponds to at least 0.6 × 10⁶ bacterial cells per worm of (fixed) 6 mm length, a figure that underlines the high nutritive importance of the bacteria in this symbiotic association. This importance is also endorsed by the percentage of bacteria in digestion (on average 8–10%, up to 24%) by the phagocytotic epidermal cells of the host. The symbiosis always involves two different morphological types of bacteria, apparently without intermediate stages. Detailed biometrical analyses demonstrate the significantly different size ranges of the two morphotypes, even though in two of the species, the normally rod-shaped Type S-bacteria are much longer than usual. About 1% of the larger, oval ‘Type L’ is regularly found in division; in some sections, this value can reach 11%. Formation of sulfur-containing globules in this type was proven by histochemical analysis. The trophic relevance of the symbiosis is considered. Zoogeographical and evolutionary implications of the observed consistency in the symbiotic pattern in all the species studied are discussed.     

Diversity and zoogeography of marine Tubificidae (Annelida,Oligochaeta) with notes on variation in widespread species

The specific and generic diversities of the marine Tubificidae (Annelida, Oligochaeta) of the NE Pacific are compared to those of the NE and NW Atlantic as well as to those of Heron Island, Australia. Diversity in the NE Pacific is relatively high when compared to that of the NE Atlantic. The Tubificidae of the NW Atlantic (limited to the eastern coast of the USA) show two distinct zoogeographic regions: Florida to Cape Hatteras; Cape Hatteras to Massachusetts. Diversity, both in terms of the number of species and number of genera, is approximately the same in these two regions, and is similar to that of both the NE Pacific and Heron Island. Evidence suggests that the widespread marine species, in particular Tubificoides pseudogaster, have a range of morphotypes across their distributions. The apparent wide distributions of these species may be due to a taxonomy unable to resolve the differences between the morphotypes. The tubificid oligochaete fauna of the NE Atlantic appears impoverished compared to the other regions examined. The NE Pacific, NW Atlantic, and Heron Island regions are not dominated by one group of species while the NE Atlantic fauna is dominated by Tubificoides benedeni and Clitellio arenarius.     

A generic revision of the Phallodrilinae (Oligochaeta, Tubificidae)

The generic classification of the subfamily Phallodrilinae (with a total of 252 species) is revised according to phylogenetic principles. Morphological character patterns are assessed under the principle of maximum parsimony, but due to the poor resolution and instability in the resulting cladograms, the analysis is supplemented with intuitive weighting of synapomorphic similarities. Thirty-one genera are recognized. The former definition of the type genus Phallodrilus Picrantoni, 1902, is revised and the members of this genus are reclassified into 20 taxa, each hypothesized to be monophyletic: Phallodrilus s.str . (revised to contain the type species only), Somalidrilus gcn.n., Milliganius gen.n., Phallodriloides gen.n., Albanidrilus gen.n., Abyssidrilus gen.n., Paraktedrilus gen.n., Uniporodrilus Erséus, 1979, Inermidrilus gen.n., Gianius gen.n., Mexidrilus gen.n., Peosidrilus Baker & Erséus, 1979, Atlantidrilus Erséus, 1983, Thalassodrilus Brinkhurst, 1963, Pirodrilus gen.n., Pirodriloides gen.n., Marionidrilus gen.n., Pectinodrilus gen.n., Pacifidrilus gen.n. and Pseudospiridion gen.n. Nine new species are described from the Northwest Atlantic: Phallodriloides pinnulatus sp.n., Abyssidrilus opulentus sp.n., A. potens sp.n., A. altoides sp.n., Mexidrilus obtusus sp.n., Peosidrilus dalei sp.n., P. aduncus sp.n., P. riseri sp.n., and Atlantidrilus hamulus sp.n. The genus Discordiprostatus Baker, 1982, is synonymized with Nootkadrilus Baker, 1982.     

Taxonomy and new bacterial symbioses of gutless marine Tubificidae (Annelida, Oligochaeta) from the Island of Elba (Italy)

In shallow sublittoral sediments of the north-west coast of the Island of Elba, Italy, a new gutless marine oligochaete, Olavius ilvae n. sp., was found together with a congeneric but not closely related species, O. algarvensis Giere et al., 1998. In diagnostic features of the genital organs, the new species differs from other Olavius species in having bipartite atria and very long, often folded spermathecae, but lacking penial chaetae. The Elba form of O. algarvensis has some structural differences from the original type described from the Algarve coast (Portugal). The two species from Elba share characteristics not previously reported for gutless oligochaetes: the lumen of the body cavity is unusually constricted and often filled with chloragocytes, and the symbiotic bacteria are often enclosed in vacuoles of the epidermal cells. Regarding the bacterial ultrastructure, the species share three similar morphotypes as symbionts; additionally, in O. algarvensis a rare fourth type was found. The divergence of the symbioses in O. algarvensis, and the coincidence in structural and bacteria-symbiotic features between the two taxonomically different, but syntopic host species at Elba are discussed.     

A revision of Lycodrilus phreodriloides (Oligochaeta, Tubificidae)

The taxon Lycodrilusphreodriloides Michaelsen, 1905 is fully described for the first time. It is now recognized as Baikalodrilus phreodriloides (Michaelsen) comb.n., a member of the Tubificidae. This is the last of the original Lycodrilus species to be reclassified.     

Ultrastructure of the Tubificid Acrosome (Annelida, Oligochaeta)

The later morphogenesis of the acrosome of Limnodriloides winckelmanni and Rhyacodrilus arthingtonae is compared with that in Enchytraeus and in earthworms. After superposition of the acrosome on the tip of the nucleus the manchette continues apically beyond the nucleus to ensheath the acrosomal tube. At the posterior limit of, and probably contained in, the spacious/ terminal primary acrosomal vesicle is an electron-dense ring. A domed protrusion into the floor of the primary vesicle is tentatively regarded as the secondary acrosome vesicle. The axial rod when first observed is attached to the vesicle complex. Later, the rod detaches and extends deeply into the acrosome tube. A membrane ensheathes the tubificid axial rod but its exact homology with the complex layers surrounding the lumbricid or megascolecid axial rod is not clear. The domed apical region of the tubificid acrosome is probably a persistence of the primary acrosome vesicle and it is deduced that the acrosome vesicle surrounding the axial rod in lumbricids and megascolecids is a product, by invagination, of the secondary acrosome vesicle only.     

Quantitative observations on the population ecology of Branchiura sowerbyi (Oligochaeta,Tubificidae)

Cohorts of Branchiura sowerbyi were reared at different temperatures and initial population densities in order to obtain data suitable for the interpretation of population dynamics in field populations. Percent hatching from cocoons reaches its maximum at 25 °C and decreases towards lower and higher temperatures. Embryonic development time, T_E, was measured and the relative threshold temperature, 10 °C, calculated by extrapolation. The degree day requirement for embryo development is 195 °C d. The time of first cocoon laying (T_gm) was observed and the ratio T_E/T_gm was seen to fit with that of other tubificid species cultured so far. Embryo mortality is rather high, while worm mortality is low or very low. Fecundity increases from 15 to 20 °C but decreases at 25 °C. A mathematical model for the simulation of population densities with four size-stage compartments is suggested. It could be used for the optimization of worm uptake (simulated as stage specific mortality) in mass cultures reared for the production of Branchiura, to be used as food for fish fingerlings.     

Iodination activity in Eisenia foetida (Annelida,Oligochaeta)

Summary In the nervous system of the earthworm Eisenia foetida, we have previously found thyroglobulin-like immunoreactive neurons. In the present study iodination activity was investigated by injecting worms or incubating them in vivo with radioiodine; animals treated with methimazole (MMI), an inhibitor of peroxidase-catalyzed iodination, served as controls. Radioiodinated proteins were identified in soluble extracts from ¹²⁵I-incubated animals; the sedimentation pattern of soluble proteins from cephalic segments showed a peak of radioactivity in the 3–4 S region. In animals pretreated with 10^-3 M MMI for 48 h, ¹²⁵I-incorporation into soluble proteins from cephalic segments was drastically reduced. Light-microscopic autoradiographic studies showed silver-grains selectively concentrated in the brain and ventral nerve cord of ¹²⁵I-injected animals. The highest grain-density occurred in the cerebral ganglion beginning 5 min after tracer injection; the reaction product was mainly distributed between the neurosecretory cells and neuropile fibres in the zone of the presumptive plexiform neurohaemal complex. In MMI-pretreated animals the reaction product was not visible in either cerebral ganglion or ventral nerve cord. Of interest, the setae appeared consistently positive with or without MMI treatment. These observations indicate that protein iodination involving peroxidase occurs in the nervous system of earthworms and suggest that iodination mechanisms, other than peroxidase-catalyzed, may be operating in some scleroprotein structures such as setae.     

Morphogenesis of the Genital Ducts and Spermathecae in Clitellio arenarius, Heterochaeta costata, Tubificoides benedii (Tubificidae) and Stylaria lacustris (Naididae) (Annelida, Oligochaeta)

The development of the male genital ducts in Clitellio arenarius, Tubificoides benedii, Heterochaeta costata (Tubificidae) and Stylaria lacustris (Naididae) is studied with the purpose of investigating the homologies between different parts of the ducts. In both Tubificidae and Naididae, the male duct comprises a funnel, a vas deferens and an atrium. There may also be a prostate gland (diffuse or compact) in association with the duct. The funnel and vas deferens, in all four species, originate from the peritoneal (mesodermal) cells in the posterior septa in the testes segment, whereas the atrium develops from an epidermal (ectodermal) invagination. The prostate glands have different origins in different taxa; in S. lacustris it differentiates from the peritoneal (mesodermal) cells surrounding the atrium, but in H. costata and T. benedii it develops by a multiplication of the atrial (ectodermal) cells; C. arenarius lacks a prostate gland. The development of the spermathecae and the female duct is also studied. The spermatheca is an epidermal invagination. The female duct is of mesodermal origin. However, the position of the duct differs; in S. lacustris the female duct is lateral and the pore is in the ovarian segment, while in the tubificids studied the duct is ventral with the pore in the segment behind the one containing the ovary.     

Cladistic analysis of the subfamilies within the Tubificidae (Oligochaeta)

A hypothesis of phylogenetic relationships within the family Tubificidae is presented, based on a Wagner analysis of morphological characters in the different subfamilies. Two major lincages are recognized. One, including the subfamilies Tubificinae, Telmatodrilinae and Limnodriloidinae, is supported by a synapomorphic ability to form slender spermatozeugmata in the spermathecae; the other, including Rhyacodrilinae (paraphyletic), Phallodrilinae, and the (present family) Naididae, is supported by two synapomorphics, the possession of modified penial setae and numerous coelomocytes (the latter secondarily lost in the Phallodrilinae). Some implications for the classification of the Tubificidae are discussed.     

Life-cycle and karyology of Branchiura sowerbyi Beddard (Oligochaeta,Tubificidae)

Data on the life-cycle of a population of Branchiura sowerbyi Beddard in a water-lily tank at the Botanical Garden in Padua are reported. The breeding period is from April to July, after which the reproductive system is partially resorbed (August–September) and reformed later in the autumn. The karyology of the species was also studied, and revealed 38 mitotic chromosomes in the gonia, and 19 bivalents in the primary spermatocytes and in the primary oocytes.     

Taxonomic Revision of the Marine Genus Heterodrilus Pierantoni (Oligochaeta,Tubificidae)1

Marine tubificids possessing trifid anterior setae are morphologically and taxonomically reviewed, on the basis of material from the Atlantic and Pacific Oceans. Heterodrilus Pierantoni, 1902 is revised to include thirteen species, H. arenicolus Pierantoni, 1902, H. minisetosus sp.n.H. ascensionensis sp.n. H. queenslandicus (Jamieson, 1977), H. lacertosus sp.n. H. scitus sp.n. H. keenani sp.n. H. claviatriatus sp.n. H. subtilis (Pierantoni, 1917), H. jamiesoni sp.n. H. occidentalis sp.n. H. pentcheffi sp.n. and H. bulbiporus sp.n. The genus is briefly defined: marine tubificids with trifid setae in preclitellar segments (with H. subtilis as the only exception); paired spermathecae located in segment X; vasa deferentia entering apical, ental ends of slender, ciliated atria, which bear broadly attached masses of prostate glands; paired male pores, and generally with penial setae arranged in bisetal bundles. Heterodriloides gen.n. is established for H. quadrithecatus sp.n. distinguished from Heterodrilus by two main features: its spermathecae are located in XII, with a supplementary pair generally located in XI; and its vasa enter the ectal part of the atria. Giereidrilus gen.n. a third genus with trifid setae, is established to include Phallodrilus ersei Giere, 1979 and G. inermis sp.n. Both species have unpaired spermathecal and male pores, and their atria are not ciliated. Heterodrilus, Heterodriloides and Giereidrilus are placed in the subfamily Rhyacodrilinae Hrabě, 1963.     

Field and Experimental Studies on the Effects of a power station effluent on tubificidae (Oligochaeta,Annelida)

1. Higher numbers of sexually mature worms of L. hoffmeisteri were found in the River Trent downstream from Drakelow Power Stations than upstream.
2. The condenser effluent from the power stations not only increased the temperature of the river but also produced a considerable increase in the concentration of dissolved oxygen.
3. Experiments were therefore carried out on the effects of these two variables on the reproductive rate of the worms.
4. In these experiments it was found that: (a) L. hoffmeisteri increased its rate of egg production with increase in temperature up to about 25°C while T. tubifex maintained a fairly steady rate of egg production over a range of temperatures from 10–25°C. (b) L. hoffmeisteri maintained a fairly steady rate of egg and cocoon production over a wide range of oxygen concentrations above 2 ppm.
5. Therefore it seems likely that the difference between the numbers of sexually mature L. hoffmeisteri upstream and downstream from the power station were influenced more by the increased temperature, than the increased oxygen levels of the power station effluent, though under extreme conditions of deoxygenation, aeration of the river by the cooling towers at the power stations could increase the abundance of this species.

     

Population dynamics of Tubificoides amplivasatus (Oligochaeta,Tubificidae) in the Oresund,Denmark

A two year fortnightly collection of data from the 27 m station in the Oresund on the tubificid species Tubificoides amplivasatus was analyzed for population trends and life stages. Recruitment patterns from year to year were consistent in timing but very irratic in magnitude, being similar to patterns seen in other estuarine and marine annelids. Sexually mature T. amplivasatus were found throughout the study period, but mature mated specimens were more abundant during late summer and autumn. It is estimated that from 120 to 150 days is spent, by this species, in the cocoon and individuals may reach maturity in less than one year. There was some indication of individuals with regressed genital organs indicating that they may live longer than one year. At the 27 m station T. amplivasatus is part of a complex and well developed benthic community. Temporal variation in this species was highly correlated to that of other major taxa (bivalves, ophiuroids).     

Caudal regeneration in Tubifex tubifex (Oligochaeta, Tubificidae) following copper exposure

Abstract. The oligochaete, Tubifex tubifex (Oligochaeta, Tubificidae), is capable of the auto-tomization and regeneration of missing body parts. The posterior end of the worm is subject to autotomy (e.g., after predation or after exposure to toxic substances) and can be regenerated thereafter. Despite the ecological importance of T. tubifex , processes of autotomy and regeneration have been little studied. This work describes daily morphological and histological observations of caudal regeneration of this worm. We also compared regeneration processes when autotomy was induced by artificial transsection of the worms (control worms) and by exposure to copper ion, a frequently encountered environmental contaminant. The worms regenerated a functional posterior end (defecation possible) in 7 d as well as a prepygidial zone from which new segments could be regenerated. In T. tubifex , regeneration involved the presence of activated mesoblastocytes in the worm, increased number of neoblasts, and the increased migration of these cells. However, Cu²⁺ did not affect these processes, since no difference could be detected between regeneration of control and Cu-autotomized worms.     

Molecular evidence for the non-monophyletic status of Naidinae (Annelida, Clitellata, Tubificidae)

Naidinae (former Naididae) is a group of small aquatic clitellate annelids, common worldwide. In this study, we evaluated the phylogenetic status of Naidinae, and examined the phylogenetic relationships within the group. Sequence data from two mitochondrial genes (12S rDNA and 16S rDNA), and one nuclear gene (18S rDNA), were used. Sequences were obtained from 27 naidine species, 24 species from the other tubificid subfamilies, and five outgroup taxa. New sequences (in all 108) as well as GenBank data were used. The data were analysed by parsimony and Bayesian inference. The tree topologies emanating from the different analyses are congruent to a great extent. Naidinae is not found to be monophyletic. The naidine genus Pristina appears to be a derived group within a clade consisting of several genera (Ainudrilus, Epirodrilus, Monopylephorus, and Rhyacodrilus) from another tubificid subfamily, Rhyacodrilinae. These results demonstrate the need for a taxonomic revision: either Ainudrilus, Epirodrilus, Monopylephorus, and Rhyacodrilus should be included within Naidinae, or Pristina should be excluded from this subfamily. Monophyly of four out of six naidine genera represented by more than one species is supported: Chaetogaster, Dero, Paranais, and Pristina, respectively.     

The species-area relationship of European Lumbricidae (Annelida,Oligochaeta)

Summary Studies throughout Europe reporting species lists of lumbricid earthworms and ranging from 100 m² to >500000 km² are analysed for the regression of species number S on size of area A [km²]. This species-area relation is described by: S=7.9*A ^0.09 (r=0.76).Revised version of a poster presented at the Wilhelm Michaelsen Memorial Symposium (International Symposium on Terrestrial Oligochaeta), Hamburg Sept. 14–18th 1987