Intra- and interspecific predation on the cocoons of Erpobdella octoculata (L.) (Annelida: Hirudinea)

In laboratory experiments, eleven out of twenty-one invertebrate species and all of the three fish species tested fed on freshly laid flaccid cocoons of Erpobdella octoculata, though predation was only severe from a dytiscid beetle, E. octoculata and the fish species. There was a tendency for more cocoons to be eaten by starved than fed predators. Only snail species damaged one-week-old tougher cocoons.Only one out of 471 E. octoculata collected during their breeding season from the stony shores of two eutrophic lakes had a cocoon in its gut.The role of cannibalism of and interspecific predation on cocoons in the control and regulation of lake-dwelling populations of the erpobdellid is discussed, and assessed to be relatively unimportant. A more likely regulatory mechanism may involve high juvenile mortality from as yet unknown causes.     

Germ-line cysts are formed during oogenesis in Erpobdella octoculata (Annelida,Clitellata, Erpobdellidae)

Abstract

Erpobdella octoculata (Clitellata, Hirudinea, Erpobdellidae) has paired ovarian sacs, each containing several rod-shaped structures termed ovarian bodies. Oogenesis takes place within the ovarian bodies. We show that in the apical part of the bodies the germ-line cells form syncytial cysts of cells interconnected by stable intercellular bridges. Germ-line cyst architecture is broadly similar to that of other clitellate annelids; that is, each germ cell has only one intercellular bridge connecting it to the anuclear cytoplasmic mass, the cytophore. Unlike germ-line cysts described in other leech species, the cytophore in cysts of E. octoculata is poorly developed, taking the form of thin cytoplasmic strands. Oogenesis in E. octoculata is meroistic because the germ cells forming the cysts (cystocytes) have diverse fates, i.e., nurse cells and oocytes appear. One large ramified cell (apical cell) occurs within the apical part of the ovarian body. We compare the ultrastructure of the apical cell found in E. octoculata with that of apical cells described recently in some hirudiniform leeches. The germ-line cysts as well as the oocytes are enveloped by somatic follicular cells. As in other leeches, the follicular cells surrounding the growing oocytes have cytoplasm perforated by intracellular canals. In view of the many similarities between E. octoculata ovarian bodies and the ovary cords described in glossiphoniids and especially in hirudiniform leeches, we suggest that the ovarian bodies found in E. octoculata are in fact modified ovary cords.     

Ultrastructure and development of the nephridia in Anaitides mucosa (Annelida,Polychaeta)

Different developmental stages (trochophores, nectochaetae, non-mature and mature adults) of Anaitides mucosa were investigated ultrastructurally. A. mucosa has protonephridia throughout its life; during maturity a ciliated funnel is attached to these organs. The protonephridial duct cells are multiciliated, while the terminal cells are monociliated. The single cilium is surrounded by 14 microvilli which extend into the duct lumen without coming into any contact with the duct cells. Corresponding ultrastructure and development indicate that larval and adult protonephridia are identical in A. mucosa. Differences between various developmental stages can be observed only in the number of cells per protonephridium. A comparison between the funnel cells, the cells of the coelothel and the duct cells reveals that the ciliated funnel is a derivative of the duct. Due to the identical nature of the larval and postlarval protonephridia, such a funnel cannot be a secondary structure. In comparison with the mesodermally derived metanephridial funnel in phoronids it seems likely that the metanephridia of annelids and phoronids evolved convergently.     

Erpobdella (Dina) parva complex (Annelida: Hirudinea: Arhynchobdellida: Erpobdellidae): additional description of Erpobdella parva, E. dubia, and E. lahontana and taxonomic revision

Erpobdella (Dina) parva complex (E. parva, E. dubia, and E. lahontana) were analyzed by species distribution, pigmentation, size, number and position of the labial eyes, tubercle presence, annulus width, gonopore position, and male genital atrium shape. I concluded that E. parva and E. dubia are conspecific, with the priority name of E. parva. The Lahontan basin species (E. lahontana), was found to be distinct by gonopore position, and now includes two additional basins (Granite Springs and Winnemucca). Endemism occurred in the Relict Dace basin complex (Butte and Steptoe basins) with respect to one form of gonopore positions. The variation in pigmentation, eye position and number, gonopore position, and male genital organ shape were highly variable in the Great Basin. Examination of the annular widths did not give any guidance to the taxonomic problem of the genera of this complex. It was noted that the Erpobdella parva complex did have some similarities with Nephelopsis obscura.     

Specialized pelagic feeding by Erpobdella montezuma (Hirudinea)

The pelagic amphipod, Hyalella montezuma comprised nearly 90% of the diet of the leech, Erpobdella montezuma in the near thermally constant environment of Montezuma Well, Arizona. This restricted diet, confirmed by both gut content and serological analyses, occurred even though other potential prey were abundant throughout the year in the pelagic column, littoral vegetation and sediments. Seasonal electivity indices for this pelagic prey species were ≥0.9. It is suggested that the highly predictable environmental conditions in Montezuma Well have contributed to this very close predator–prey relationship.     

Ultrastructure of the anterior salivary gland cells of the giant leech, Haementeria ghilianii (Annelida, Hirudinea)

The giant anterior salivary gland cells from the large mammalian blood-sucking, glossiphoniid leech, Haementeria ghilianii, can be subdivided into three morphologically and functionally distinct regions: 1) a soma, responsible for the synthesis and storage of secretory products; 2) a long cell process, responsible for the storage and intracellular transport of the secretory vesicles; and 3) the site of exocytosis at the process terminal. The giant somata are densely packed with secretory vesicles. Deep plasmalemmal invaginations invade the soma and form an extensive system of extracellular lacunae. The rough endoplasmic reticulum (ER) and the Golgi apparatus are organized in the cell periphery, near the highly branched nucleus, and along the lacunae. The somata taper into long processes extending over several centimeters to the proboscis tip. These contain secretory vesicles through their whole length. In the process periphery, the vesicles are completely ensheathed by a concentric subplasmalemmal smooth ER cisterna. This originates deeply within the soma and extends through the whole cell process to its terminal. The ER provides support for up to several hundred longitudinally oriented microtubules. Secretion occurs at the very tip of the cell processes, each of which terminates at the proboscis tip at the base of a cuticular pore. We found synapses close to the sites of exocytosis, providing morphological evidence for neuronal control of secretion.     

Structure and development of the nephridia of Tomopteris helgolandica (Annelida)

 Nephridial diversity is high in Phyllodocida (Annelida) and ranges from protonephridia to metanephridia. The nephridia of Tomopteris helgolandica (Tomopteridae) can be characterized as metanephridia which bear a multiciliated solenocyte. This cell is medially apposed to the proximal part of the nephridial duct and bears several cilia, each of which is surrounded by a ring of 13 microvilli. An extracellular matrix connects the microvilli and thus leads to the impression of a tube surrounding the central cilium. Each tube separately enters a subjacent duct cell and the cilia extend into a cup-shaped compartment within the duct cell. This compartment is not connected to the duct. The funnel consists of eight multiciliated cells and is connected to the nephridial duct, which initially runs intercellularly and later percellularly. The last duct cell bears a neck-like process which pierces the subepidermal basal membrane and is connected to epidermal cells forming a small invagination, the nephropore. The nephridia of T. helgolandica develop from a band of cells and all structural components are differentiated at an early developmental stage. Further development is characterized by enlargment of the funnel, ciliogenesis in the solenocyte, merging of different sections of the duct and, finally, the formation of the nephropore. An evaluation of the nephridia of T. helgolandica leads to the hypothesis that the nephridial diversity in Phyllodocida can be explained by the retainment of different stages in the transition of protonephridia into metanephridia; this is caused by the formation of a ciliated funnel at different ontogenetic stages. Although the protonephridia in Phyllodocida are regarded as primary nephridial organs, protonephridia are also presumed to have evolved secondarily in progenetic interstitial species of the Annelida by an incomplete differentiation of the nephridial anlage. Accepted: 18 December 1996     

Morphology and ultrastructure of the midgut in Piscicola geometra (Annelida, Hirudinea)

This paper presents information on the organization of the midgut and its epithelium ultrastructure in juvenile and adult specimens of Piscicola geometra (Annelida, Hirudinea), a species which is a widespread ectoparasite found on the body and gills and in the mouth of many types of fish. The analysis of juvenile nonfeeding specimens helped in the explanation of all alterations in the midgut epithelium which are connected with digestion. The endodermal portion (midgut) of the digestive system is composed of four regions: the esophagus, the crop, the posterior crop caecum, and the intestine. Their epithelia are formed by flat, cuboidal, or columnar digestive cells; however, single small cells which do not contact the midgut lumen were also observed. The ultrastructure of all of the regions of the midgut are described and discussed with a special emphasis on their functions in the digestion of blood. In P. geometra, the part of the midgut that is devoid of microvilli is responsible for the accumulation of blood, while the epithelium of the remaining part of the midgut, which has a distinct regionalization in the distribution of organelles, plays a role in its absorption and secretion. Glycogen granules in the intestinal epithelium indicate its role in the accumulation of sugar. The comparison of the ultrastructure of midgut epithelium in juvenile and adult specimens suggests that electron-dense granules observed in the apical cytoplasm of digestive cells take part in enzyme accumulation. Numerous microorganisms were observed in the mycetome, which is composed of two large oval diverticles that connect with the esophagus via thin ducts. Similar microorganisms also occurred in the cytoplasm of the epithelium in the esophagus, the crop, the intestine, and in their lumen. Microorganisms were observed both in fed adult and unfed juvenile specimens of P. geometra, which strongly suggests that vertical transmission occurs from parent to offspring.     

Egg-feeding in the freshwater piscicolid leech Cystobranchus virginicus (Annelida, Hirudinea)

Abstract. Leeches are common terrestrial and aquatic annelids, parasitizing or feeding on a wide range of host taxa. Here we report evidence for an unusual feeding behavior of egg‐feeding in the piscicolid leech Cystobranchus virginicus. We identified distended specimens of C. virginicus in the nests of at least 4 different fish species: Campostoma anomalum, Moxostoma carinatum, Moxostoma sp. (either M. anisurum and/or M. breviceps), and Nocomis leptocephalus. We collected a total of 41 leeches from the nests of these host species and documented at least 1 leech in 19 of 55 nests (35%), with many sites containing multiple leeches. Individuals of C. virginicus were not identified feeding on any of the 41 adult specimens of Moxostoma spp. or the 635 adult specimens of Nocomis leptocephalus examined, and were never found in the absence of active host spawning (26 sites). These results are consistent with individuals of C. virginicus being an opportunistic or possibly even an obligate egg‐feeder, potentially timing their own reproductive activities with the spawning of their fish hosts. The current distribution of C. virginicus has been expanded to include North Carolina, South Carolina, and Tennessee. The potential for leech species to induce mortality in developing fish eggs could be a concern for fish conservation and merits further investigation.     

The Natural Feeding and Resource Partitioning of Erpobdella octoculata L. and Erpobdella testacea SAV. in Lake Esrom,Denmark

The natural feeding and competitive interactions between populations of Erpobdella ostoculata and Erpobdella testacea were investigated in Lake Esrom, Denmark, during 1979/80. Statistical analysis revealed that the size of the leeches was the main factor involved in resource utilization. Size-specific feeding included differences in the numerical composition of diets and the size of individual prey. Five weight classes of Erpobdella spp. were distinguished. The number of prey per leech increased from 1.63-2.84 for the first to the fifth weight class, whereas diversity in feeding averaged 1.71 prey per leech. Quantification of competitive interactions indicated that the temporal differences in weight class composition of the two species were sufficient to explain coexistence, although both species have an annual life cycle, and neither species showed taxonomic food refuges.     

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.     

The complete mitochondrial genome sequence of Whitmania pigra (Annelida, Hirudinea): the first representative from the class Hirudinea

The mitochondrial genome is a significant tool for investigating the evolutionary history of metazoan animals. The currently available mitochondrial genome data in GenBank is limited to understand the detail evolutionary relationship among the metazoan animals, especially in the phylum Annelida. Here we present the mitochondrial gene organization, gene order and codon usage of the leech Whitmania pigra (Annelida), which is the first representative from the class Hirudinea. It is a circular molecule of 14,426bp, and encodes 13 protein-coding genes, 2 ribosomal RNA genes, and 22 transfer RNA genes. All 37 genes of W. pigra mitochondrial genome are transcribed from the same strand, which is identical to studied annelids, two echiurans, two sipunculans and many other lophotrochozoans. Five conserved gene clusters can be found in mitochondrial genomes of nine studied annelids, including (1) cox1-N-cox2; (2) cox3-Q-nad6-cob-W-atp6; (3) H-nad5-F-E-P-T-nad4L-nad4; (4) srRNA-V-lrRNA; and (5) nad3-S(1)-nad2. Compared with that of other studied annelids, translocations of transfer RNAs were found in the gene arrangement of W. pigra mitochondrial genome. Phylogenetic analysis strongly support that the species from Hirudinina and Oligochaeta form a monophyletic group Clitellata (BPM=100, BPP=100), which is consistent with previous research based on morphological and other molecular data. Both gene order data and amino acid sequences reveal that echiurans are derived annelids and sipunculans should be clustered with annelids and echiurans.     

Topographie des kreislaufsystems und zirkulation bei Hirudo medicinalis (Annelida,Hirudinea)

The circulatory system of the leech Hirudo medicinalis was investigated by means of the latex method and in vivo experiments. For the first time the vascular configuration of the suckers and nephridia, and a unidirectional blood flow in all vessels are demonstrated.

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Mit Unterstützung der Deutschen Forschungsgemeinschaft.     

Structure of the vector tissue in piscicolid leeches (Annelida, Hirudinea, Rhynchobdellida, Piscicolidae)

Hypodermic insemination occurs in piscicolid leeches (Hirudinea, Rhynchobdellida, Piscicolidae). The spermatophore is implanted in a specialized region of the leech body, the copulatory area. Just beneath the copulatory area, there is a specialized connective tissue (vector tissue) that is considered to guide the sperm toward the ovaries. In this study, we show that the vector tissue in the four species of the genus Piscicola is composed of a mass of cells located directly beneath the copulatory area, and two thin strands extend toward the ovaries. The ultrastructure of the vector tissue has been described for the first time. Four cell types were identified, constructing the vector tissue. The envelope of this tissue is made up of extracellular fibrous matrix and two types of cells: vesicular and flat envelope cells, which are embedded within the matrix. The rest of the tissue is formed of granular and plasmatic cells. Both of these last cell types have prominent cytoplasmic projections, filled with a filamentous material. However, only granular cells have numerous small electron-dense granules in their cytoplasm. The vector tissue was described prior, during and following copulation. Sperm passes within free spaces between the granular and plasmatic cells. Characteristic vector tissue cells also occur within the ovary wall and inside the ovary lumen. This supports earlier data, which postulated that the vector tissue appears to be an outgrowth of the ovary wall.     

The Feeding Strategies of the Leech Erpobdella octoculata (L.): A Laboratory Study

The feeding behaviour of the freshwater leech Erpobdella octoculata was analysed by exposing potential invertebrate and vertebrate prey organisms (alive, wounded or dead) to leech attack in dishes, in the laboratory. The fact that E. octoculata is a macrophagous feeder that swallows living prey organisms whole (preferentially Chironomus larvae) is documented. However, it was repeatedly observed that adult leeches sucked the body fluids from wounded larvae. Likewise, cut pieces of earthworms, dead crustaceans and crushed water snails were attacked and the soft parts sucked in with the aid of the unarmed pharynx. Adult leeches sucked the body fluids from dead, decaying bodies of vertebrates (fish, newt larvae). Newly hatched young are blood suckers that rapidly attacked the wounded regions of Chironomus larvae and other invertebrates such as crushed water snails. It is concluded that the common leech E. octoculata is not only a predator, but also a fluid sucker and a scavenger. The ecological implications of this finding are discussed.     

Diet of the leeches Erpobdella octoculata (L) and Helobdella stagnalis (L) in a lotic habitat subject to organic pollution

SUMMARY 1. A study of the diet of E. octoculata (L) and H. stagnalis (L) using a serological technique was carried out in a lot ic habitat subject to organic pollution and seasonal sewage fungus growth.
2. The results indicate that E. octoculata consumed predominantly Chironomidae and Oligochaeta, while H. stagttalis had a less pronounced prey preference, consuming rather similar proportions of chironomids, oligochaetes, Asellus and gastropod snails.
3. At enriched sites, E. ocioculata consumed relatively more chironomids and fewer oligochaetes, while H. stagnalis took more gastropods and fewer chironomids.
4. Seasonal differences were noted in the diet of both leeches with chironomids predominating chiefly from April to August, and molluscs, oligochaetes and Asellus at other times of the year. Intra-specific differences (on a weight-age basis) were only seen for E. octoculata , small forms consuming chiefly oligochaetes and larger ones concentrating on chironomids.     

Dystrophin-associated proteins in obliquely striated muscle of the leech Pontobdella muricata (Annelida, Hirudinea)

The distribution of dystrophin-associated proteins (-dystroglycan, -, -, - and -sarcoglycan, -syntrophin and sarcospan) were studied in obliquely striated muscle of the leech Pontobdella muricata. Western blot analysis and immunohistochemical electron microscopy, using various polyclonal antibodies, were employed. Western blot analysis of all of these antibodies showed a single band, with approximately the same molecular weights as similar proteins detected in vertebrate muscles. The immunoelectron microscopy study confirmed specific immunogold labelling in the membrane of muscle cells. Since all dystrophin complex components have similar molecular weights and the same localisation in leech as in vertebrate skeletal muscle, we assume that these proteins have similar properties in leech and vertebrate muscle. The presence of these molecules in annelid muscles, together with a short version of dystrophin (previously described as IDLp-140) is of particular interest since phylogenetic and functional studies on this material could help to shed new light on the role and function of this complex in the muscle membrane.     

Prey location and prey choice by the freshwater leech Erpobdella octoculata using foraging kairomones

1. The freshwater leech, Erpobdella octoculata , is a generalist predator feeding on prey organisms such as Tubifex spp., Chironomus spp. and Asellus aquaticus. Using different experimental designs, we studied the use of foraging kairomones by the leeches for prey location.
2. Leeches were attracted to living as well as to freshly killed larvae of Chironomus sp., to Tubifex sp., and to A. aquaticus offered in Petri dishes covered with gauze. The leeches also reacted to an extract of macerated Tubifex sp. presented in agar.
3. Using ion exchange chromatography, the presence of histidine and glutamic acid was demonstrated in water contaminated by living larvae of Chironomus sp. and Tubifex sp. Agar blocks containing a synthetic mixture of these compounds at concentrations above 5 mg mL⁻¹ were attractive to the leeches.
4. Choice tests showed that leeches preferred chemical signals from Tubifex sp. over larvae of Chironomus sp. No difference was found between chemicals from Tubifex sp. and A. aquaticus , and A. aquaticus and larvae of Chironomus sp.
5. The results demonstrate that E. octoculata uses specific foraging kairomones in searching for prey and indicate that amino acids serve as foraging kairomones.