Are the lake-dwelling leeches,Glossiphonia complanata (L.) and Helobdella stagnalis (L.), opportunistic predators on molluscs and do they partition this food resource?

SUMMARY. 1. Predation on the mollusc genera Potamopyrgus, Bithynia, Valvata, Lymnaea, Physa, Planorbis and Pisidium by the leeches Glossiphonia complanata (L.) and Helobdella stagnalis (L.) was examined in five eutrophic lakes at monthly intervals over one year using a serological technique.
2. Feeding intensity varied seasonally, being lowest in winter and highest in summer. Small, medium and large leeches preyed to the same extent on the several mollusc genera; this was true for both leech species. Qualitatively, the diet of both glossiphoniids was similar throughout the year. Snail genera were consumed in proportion to their relative abundance in the field. Quantitatively, Glossiphonia preyed more heavily on snails than did Helobdella.
3. It is concluded that both leech species are opportunistic predators.     

Experimental observations on the specificity of Apatemon (Australapatemon) minor (Yamaguti 1933) (Digenea: Strigeidae) toward leech (Hirudinea) second intermediate hosts

The infectivity of Apatemon (Australapatemon) minor cercariae to 7 species of freshwater leech was examined under laboratory conditions. The leech species exposed to infection were; Erpobdella octoculata, Helobdella stagnalis, Glossiphonia heteroclita, Glossiphonia complanata, Hemiclepsis marginata, Piscicola geometra, and Theromyzon tessulatum. Five species were capable of acting as second intermediate hosts. Despite this broad specificity only Erpobdella octoculata and Helobdella stagnalis could be considered to show a high degree of compatibility with the parasite. In these 2 leech species more than 38% of the cercariae successfully penetrated and established metacercarial cyst infections. The leeches Piscicola geometra and Theromyzon tessulatum did not become infected. Close parallels were found between the species order of host utilization determined experimentally and that revealed by a range of field surveys in Britain, Eastern Europe and Russia. This suggests that the order of second intermediate host utilization in the natural environment has, at least in part, a physiological basis. The degree to which different leeches are utilized as hosts may relate to the opportunity which they afford for transmission of A. minor to wildfowl definitive hosts.     

Food utilization and niche overlap in three species of lake-dwelling leeches (Hirudinea)

The diets of Erpobdella octoculata, Glosiphonia complanata and Helobdella stagnalis on the stony littoral zone of eutrophic Crose Mere were examined over two years using the precipitin test. The abundances of food organisms were measured. For all leech species, juvenile mortality was greatest in locations where a low ratio of prey abundance to recruited leech abundance occurred, and the intensity of feeding by Erpobdella and Helobdella fell slightly in late summer when large numbers of juveniles of these species were present; these suggest the involvement of food in juvenile mortality, Seasonal changes in feeding intensity were similar for all leech species, with the exceptions outlined above and for Glossiphonia in April when feeding by brooding adults ceased, at which time the severity of any interspecific competition would have been reduced. Within a leech species, there was little change in the food spectrum as the leeches grew. Niche breadth was lowest for Erpobdella and highest for Helobdella. Niche overlap was greatest between Glossiphonia and Helobdella, and there was a trend for overlap values to be lower between Glossiphonia and Erpobdellu than between Helohdellu and Erpohdellu. Erpobdella fed mainly on chironomids and oligochaetes, Glossiphonia on molluscs, oligochaetes and chironomids, and Helobdella on oligochaetes, chironomids, Asellus, molluses and amphipods, all in decreasing order of importance. It is suggested that coexistence in the leech species may be due in part to Erpobdella and Glossiphonia having 'food refuges' in chironomids and molluscs, respectively, with Helobdellu being more of a general predator.     

The occurrence of metacercariae of the trematode, Cyathocotyle opaca (Wisniewski), in three species of lake-dwelling leeches

SUMMARY. 1. The leeches, Erpobdella octoculata, Glossiphonia complanata and Helobdella stagnalis , were collected at monthly intervals over a 2-year period from a eutrophic English lake, and examined for the presence of metacercariae of the trematode. Cyathocotyle opaca.
2. Only one specimen of each of H. stagnalis and G. complanata was recorded with the parasite. Seasonal changes in prevalence levels in E. octoculata were similar for each of the three cohorts identified during the study period. Values, low in young leeches recruited in the autumn, rose slowly until the following spring, and then increased more rapidly till the autumn, when the cohort died out. Mean intensity and relative density showed similar patterns of seasonal change to that of prevalence.
There was no evidence of parasite induced mortality in E. octoculata. Attainment of sexual maturity did not differ between infected and uninfected leeches.     

Hyaluronidase activity in leeches (Hirudinea)

The leech hyaluronoglucuronidase (hyaluronidase I) was identified in Erpobdellidae (Nephelopsis obscura and Erpobdella punctata) and Glossiphoniidae (Desserobdella picta) and historically described from Hirudinidae (Hirudo medicinalis). A second leech hyaluronidase (hyaluronidase II) which hydrolyzed only a few bonds to for hyaluronan oligosaccharides larger than 6500 Da, was found in Glossiphoniidae (Helobdella stagnalis, Glossiphonia complanata, Placobdella ornata, and Theromyzon sp.) and in Haemopidae (Haemopis marmorata). The distribution of the two hyaluronidases in leech occurred in both orders (Arhynchobdellida and Rhynchobdellida) and in macrophagous and haematophagous feeding types whereas the liquidosomatophagous leeches only had hyaluronidase II.     

The influence of temperature on the life cycle and occurrence of three species of lake-dwelling leeches (Annelida: Hirudinea)

The influence of constant temperatures on the growth, maturation and reproduction of field-collected and F, generation Helobdella stagnalis, Glossiphonia complanata and Erpobdella octoculata was investigated. Leech material from a lowland, productive lake and from an upland, unproductive lake was cultured at each of the temperatures: l·5,5·5,8, 10·5, 13,16, 19 and 23°C. Field-collected and F₁ generation H. stagnalis and E. octoculata matured and produced eggs and young over the range 10·5–23°C, whereas the range for egg production was 8–23°C for field-collected G. complanata, F, generation leeches failing to mature at any temperature due to an additional limiting factor being involved.
Optimal temperatures for cocoon/egg production were observed for E. octoculata, but egg production was similar at all temperatures for G. complanata and H. stagnalis. In contrast, the viability of eggs was greater at certain temperatures for the last two species but was similar at all temperatures for E. octoculata. Differences in egg production between field-collected and F, generation leeches are discussed. Rising temperatures accelerated rates of egg hatching, and of growth and maturation of leeches. The observed differences in survival of leeches at the various temperatures are discussed. Ecotypic adaptation to temperature within the small geographical area of Britain may not occur. It is concluded that though temperature may be a contributory factor determining distribution and abundance in British lakes, other causative factors, such as the occurrence and abundance of food organisms, are more likely to be implicated.     

Predation on leeches in a weedy pond

SUMMARY. 1. A range of sizes of Erpobdelta octoculata fL.), Glossiphonia complanata (L.) and Helobdella stagnalis (L.) were introduced to a small weeded pond harbouring invertebrate and amphibian predators. Control leeches were kept in protective cages. Subsequently, gut contents of potential predators were tested against three anti-leech sera, using the precipitin test. Five of fifteen species tested had fed on leeches; Agabus, Pyrrhosoma, Aeshna, Sympetrum and larval Trilurus.
2. The size distributions of introduced and surviving leeches were compared. Predation pressure had been greatest on smaller leeches and this may have accounted for the observed differential mortality between leech species.
3. It is concluded that predation may cause significant mortality in leech populations in weeded ponds, with severity determined by the types and abundance of predators present.     

The incidence of predation on lake-dwelling leeches

SUMMARY. 1. Erpobdella octoculata (L.), Glossiphonia complanata (L.) and Helobdella stagnate (L.) were eaten readily by larval and adult dytiscid beetles, larval caddisflies and Sialis , nymphal odonatans and various fish in laboratory experiments.
2. A serological technique showed that very few lake-collected specimens of these predatory taxa, plus triclads, leeches and stone fly nymphs, had been feeding on leeches.
3. A literature survey of lake studies on fish diet indicated that usually less than 6% of individuals with gut contents had eaten leeches. Few detailed records of waterfowl feeding on leeches have been documented.
4. It is concluded that predation pressure on lake-dwelling leeches is light, and is more severe from fish than invertebrates, less on populations inhabiting stony shores than in vegetation, and greater on the erpobdellid than the two glossiphoniid species.     

Diversity in Reproduction and General Morphology between Two Glossiphonia Species (Hirudinea) in Lake Esrom,Denmark*

According to Bennike (1943) the leech fauna in Lake Esrom, Denmark, includes two types of Glossiphonia complanata (L.), namely G. complanata typica Bennike, 1943 and G. complanata concolor (Apáthy, 1888). The results of the present investigation, which were based on material collected in 1975, 1976, and 1980, strongly indicated that we are dealing with two species in Lake Esrom, namely Glossiphonia complanata (L.) and G. (Clepsine) concolor (Apáthy). The two species have a rather similar life history, but G. complanata is on average larger than G. concolor. Differences in reproduction included size of eggs and timing of breeding, but the number of offspring seemed to be similar. Tank experiments revealed that all offspring of G. complanata had a conspecific parent, and likewise for G. concolor. The general appearance of the two species is significantly different, and the average ratio of body width to body height (W/H ratio) was ca. 30% higher for preserved individuals of G. complanata than for G. concolor. The ecological distribution of the two types, and the reliability of pigmentation as a diagnostical tool in leech systematics are discussed. Characters used for the identification of the species are included.     

Scanning Electron Microscopy of Gregarines (Protozoa, Sporozoa) and Its Contribution to the Theory of Gregarine Movement

SYNOPSIS. Scanning electron microscopy was used to reveal detailed surface structure of 4 septate ( Gregarina cuneata, G. steini, G. rhyparobiae, Pileocephalus blaberae ) and one aseptate species ( Nematocystis elmassiani ) of eugregarines. The epicyte of all these gregarines is differentiated into a system of regular longitudinal folds. In the septate species these folds undulate so that these organisms glide along. The undulatory pattern is absent from Nematocystis , which does not glide. The theories and the mechanism of gregarine gliding are discussed.     

The life cycle of Australapatemon magnacetabulum (Digenea: Strigeidae) from Northwestern Argentina

The life cycle of Australapatemon magnacetabulum Dubois, 1988 was resolved experimentally. Planorbid snails Biomphalaria tenagophila (d'Orbigny, 1835) collected in a small pond at the confluence of the San Lorenzo and Arias Rivers, near Salta City, Province of Salta, Argentina, were found to be shedding furcocercous cercariae possessing 4 pairs of penetration glands, 1 pair of unpigmented eyespots, 6 pairs of flame cells in the body, and 1 pair in the tail stem. Metacercariae were found encysted in naturally, and experimentally, exposed leeches Helobdella adiastola Ringuelet, 1972, Helobdella triserialis (Blanchard, 1849), Haementeria eichhorniae Ringuelet 1978, and Haementeria sp., and within their sporocysts in naturally infected planorbid intermediate hosts. Sexually mature adults were recovered from domestic chicks and a duck 8-28 days postexposure by metacercariae from leeches. The identification of the species was based upon the characteristic large ventral sucker and a genital cone, crossed by a hermaphroditic duct with internal folds, occupying approximately a 1/4 to 1/5 of the hindbody.     

The cleavage pattern in the leech Theromyzon tessulatum (Hirudinea, Glossiphoniidae)

In order to evaluate the differences in the cleavage patterns of the glossiphoniid leeches Glossiphonia complanata and Theromyzon tessulatum, previously studied by Müller ('32) and Schmidt ('17, '41), the cleavage of Theromyzon tessulatum was reexamined. For the period of the first 29 hours of development embryos were observed, photographed, and serially sectioned for light microscopy at each developmental stage. The exact cell lineage until completion of teloblast formation is reported. Besides some other not previously reported features, we show that the mesoteloblast precursor cell in the glossiphoniid leeches, as probably in most Annelida, is not the cell 3D, but cell 4d formed by an additional division of cell 3D. The results further indicate that all glossiphoniid leeches likely share a common cleavage pattern, and that major differences between Glossiphonia complanata and Theromyzon tessulatum do not exist. A comparison between the cleavage patterns of some Oligochaeta and Hirudinea is made, and plesiomorphic characters in the cleavage of a clitellate ancestor species and their deviations in present day species are discussed.     

Competition and coexistance between Glossiphonia complanata and Helobdella stagnalis (Glossiphoniidae: Hirudinoidea)

Summary The prey utilization of Glossiphonia complanata and Helobdella stagnalis from Bruce Lake, Alberta, Canada was examined quantitatively using serological techniques. While considerable prey range overlap occurred between the species, niche overlap was low during the winter, peaked in March and declined through the summer. Temporal differences in feeding and intraspecific weight class differences in prey utilization were found in both species but more distinctly in G. complanata. It is suggested that co-existance of G. complanata and H. stagnalis is based on adjustments of weight class food resource partitioning on a temporal basis.     

Molecular Characterization of Gregarines from Sand Flies (Diptera: Psychodidae) and Description of Psychodiella n. g. (Apicomplexa: Gregarinida)

ABSTRACT. Sand fly and mosquito gregarines have been lumped for a long time in the single genus Ascogregarina and on the basis of their morphological characters and the lack of merogony been placed into the eugregarine family Lecudinidae. Phylogenetic analyses performed in this study clearly demonstrated paraphyly of the current genus Ascogregarina and revealed disparate phylogenetic positions of gregarines parasitizing mosquitoes and gregarines retrieved from sand flies. Therefore, we reclassified the genus Ascogregarina and created a new genus Psychodiella to accommodate gregarines from sand flies. The genus Psychodiella is distinguished from all other related gregarine genera by the characteristic localization of oocysts in accessory glands of female hosts, distinctive nucleotide sequences of the small subunit rDNA, and host specificity to flies belonging to the subfamily Phlebotominae. The genus comprises three described species: the type species for the new genus— Psychodiella chagasi ( Adler and Mayrink 1961 ) n. comb., Psychodiella mackiei ( Shortt and Swaminath 1927 ) n. comb., and Psychodiella saraviae ( Ostrovska, Warburg, and Montoya-Lerma 1990 ) n. comb. Its creation is additionally supported by sequencing data from other gregarine species originating from the sand fly Phlebotomus sergenti . In the evolutionary context, both genera of gregarines from mosquitoes ( Ascogregarina ) and sand flies ( Psychodiella ) have a close relationship to neogregarines; the genera represent clades distinct from the other previously sequenced gregarines.     

The durations and compositions of cell cycles in embryos of the leech, Helobdella triserialis

When tritiated thymidine triphosphate ([(3)H]TTP) or its immunohistochemically detectable analogue, bromodeoxyuridine triphosphate (BrdUTP), is injected into blastomeres of leech embryos it passes throughout the entire embryo and is rapidly incorporated (within 2 min after injection) into nuclei of cells synthesizing DNA (S phase). In the same embryos a DNA-specific stain can be used to identify cells in mitosis (M phase) or nonreplicative interphase (G(1) or G(2) phase) on the basis of nuclear or chromosomal morphology. Using this procedure, we have determined the lengths and compositions of the mitotic cell cycles of identifiable cells in early embryos of the leech, Helobdella triserialis, and have analysed how the cell cycles change during the first seven stages of development. The relatively short cell cycles of the early blastomeres comprise not only phases of M and S, but also postreplicative gap (G(2)) phases. The lengthening of the cell cycles that occurs as development progresses is primarily accomplished by an increase in the length of G(2) and secondarily by an increase in the length of S and,in some instances, the addition of a prereplicative gap(G(1)) phase; M phase remains relatively constant. These data suggest that the durations of the cell cycles of embryonic cells are regulated by a variety of mechanisms.     

Lessons from leeches: a call for DNA barcoding in the lab

Many evolution of development labs study organisms that must be periodically collected from the wild. Whenever this is the case, there is the risk that different field collections will recover genetically different strains or cryptic species. Ignoring this potential for genetic variation may introduce an uncontrolled source of experimental variability, leading to confusion or misinterpretation of the results. Leeches in the genus Helobdella have been a workhorse of annelid developmental biology for 30 years. Nearly all early Helobdella research was based on a single isolate, but in recent years isolates from multiple field collections and multiple sites across the country have been used. To assess the genetic distinctness of different isolates, we obtained specimens from most Helobdella laboratory cultures currently or recently in use and from some of their source field sites. From these samples, we sequenced part of the mitochondrial gene cytochrome oxidase I (COI). Sequence divergences and phylogenetic analyses reveal that, collectively, the Helobdella development community has worked on five distinct species from two major clades. Morphologically similar isolates that were thought to represent the same species (H. robusta) actually represent three species, two of which coexist at the same locality. Another isolate represents part of a species complex (the "H. triserialis" complex), and yet another is an invasive species (H. europaea). We caution researchers similarly working on multiple wild-collected isolates to preserve voucher specimens and to obtain from these a molecular "barcode," such as a COI gene sequence, to reveal genetic variation in animals used for research.     

Comparative surface morphology of marine coelomic gregarines (Apicomplexa, Urosporidae): Pterospora floridiensis and Pterospora schizosoma

Two species in the aseptate gregarine genus Pterospora from the Pacific and Gulf coasts were analyzed by scanning electron microscopy, which revealed characteristics not reported in other gregarines. The gamonts of these species had branching trunks that ended in terminal digits, and both species moved by cytoplasmic streaming and peristalsis. Pterospora floridiensis had surface pits and tracts of parallel ridges that bended and connected with one another. Pterospora schizosoma had irregular-shaped surface swellings that were usually arranged in rosette patterns. These unique surface features have not been reported for other gregarines, and are strikingly different from the surface features of many septate and aseptate gregarines that inhabit the intestinal lumena of their hosts and move by gliding. The correlation of Pterospora's unique pellicular features to the habitat and cytoplasmic streaming characteristic of the genus may be significant, and may reflect an adaptation for development in coelomic environments.     

Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid.

ht-en protein, an annelid homolog of the Drosophila engrailed protein, is expressed during both early development and neurogenesis in embryos of the leech, Helobdella triserialis. In Helobdella as in Drosophila, early expression is in segmentally iterated stripes of cells within the posterior portion of the segment and later expression is in cells of the segmental ganglia. These findings suggest that dual expression of an en-class gene was present in a common ancestor of annelids and arthropods.     

Phylogeny and revision of the leech genus Helobdella (Glossiphoniidae) based on mitochondrial gene sequences and morphological data and a special consideration of the triserialis complex

The relationships, as well as identification of species, within Helobdella (Glossiphoniidae) were explored through phylogenetic analysis and through an overview of the historical systematics of the genus. The phylogeny was determined using morphological data and the mitochondrial gene sequences of cytochrome c oxidase subunit I and nicotinamide adenine dinucleotide dehydrogenase subunit I. A broad representation of 15 ingroup species was sampled, including 10 individuals from South America. Outgroup taxa included five species of Haementeria . Cladistic analysis of all available data resulted in one most parsimonious tree. Results shed light on genetic divergence of members classified as the same species, including those that are not monophyletic. Historically, external morphological characters have played a significant role in contributing to the confusion in the classification of H. triserialis, H. papillata, H. lineata and H. fusca in North America. Re-evaluation of Verril's Clepsine papillifera var. b and var. d in a phylogenetic context provides a solution. Additionally, the genera Adaetobdella, Acritobdella, Dacnobdella and Gloiobdella created by Ringuelet are returned to Helobdella based on overlapping morphological characters.