Changes in the parasite fauna of whiting Odontogadus merlangus L. with age and sex of host, season, and from different areas in the vicinity of the Isle of Man

Infestation of whiting with the helminths Derogenes varicus Müller, Hemiurus communis Odhner, Grillotia erinaceus Van Beneden (plerocercoids) and Contracaecum clavatum Rudolphi, and the copepod Lernaeocera branchialis L., increased with the age of the fish but infestation with the helminths Lecithaster gibbosus Rudolphi, Stephanostomum pristis Looss and Podocotyleatomon and the copepod Clavella uncinata Müller decreased as the fish aged. Infestation with the gill monogenean Diclidophora merlangi Kuhn remained at much the same level in fish 1–5+ years old. Derogenes, Hemiurus, Lecithaster, Cotracaecum and Stephanostomum showed seasonal fluctuations in the levels of their populations in whiting. In all cases the parasites reached a main peak in the summer and early autumn, a time when juvenile digeneans were most apparent.
Whiting from Morecambe Bay were less infested with Clavella than whiting taken from other areas. Experimental evidence suggests that the lower salinity of Morecambe Bay may be responsible; however, this could not account for the lower infestation of Morecambe Bay whiting by Diclidophora which appeared to be unaffected by a lowered salinity. Whiting from the east side of the Isle of Man were more infested with Lernaeocera but less infested with Diclidophora than fish from the west side of the island. The myxosporidian Myxobolus aeglefini Auerbach was externally visible in the sclera of whiting from the east side of the island but absent from the sclera of whiting from the west side of the island. It is, therefore, suggested that whiting to the east of the Isle of Man form a separate sub-stock from those to the west of the island.     

Observations on the occurrence of Diclidophora merlangi (Trematoda: Monogenea) on the gills of whiting, Gadus merlangus

Diclidophora merlangi is a common parasite of whiting in the Irish Sea. The incidence of infection over an 18-month period of study varied between 43-59%. The majority of flukes in single worm infections are found on the 1st gill arch, although in infections of higher intensity increasing numbers of parasites are found on the remaining arches. The factors which may influence the distribution of Diclidophora on the host gills are discussed.     

Spermatogenesis in a monogenean, Diclidophora merlangi.

Halton D. W. &; Hardcastle A. 1976. Spermatogenesis in a monogenean, Diclidophora merlangi. International Journal for Parasitology6: 43–53. Development of the spermatozoa in the testis of a polyopisthocotylean fish-gill fluke, Diclidophora merlangi, has been examined by light and electron microscopy. Spermatogonial cells are typically undifferentiated and display numerous free ribosomes and relatively little cytoplasm. Successive mitotic divisions produce spermatocytes which are characterized by expansion of the ER and the development of Golgi complexes. Nuclear division is followed by incomplete cytokinesis so that spermatocytes and subsequent stages are joined and develop syncytially. Nuclear synaptonemal complexes mark the first division of the meiotic phase, the second giving rise to a rosette of 32 spermatids. During spermateleosis, the spermatid nucleus condenses and migrates into a conical-shaped projection of cytoplasm. A centriole-like structure and basal bodies, anchored by a pair of attached rootlets, produce axial filaments that grow out from the spermatid and eventually fuse with the nuclear projection. Spermatozoa are then released from the residual cytoplasm. Each spermatozoon is approximately 325 μm in length and 2 μm maximum diameter and in section shows a nucleus, mitochondrion, paired axial units which conform to the “9 +1” pattern described for other platylelminthes, particles of β-glycogen, and a line of micro-tubules around the inner aspect of the limiting membrane.     

The occurrence of bacteria and mycoplasma like organisms in a monogenean parasite Diclidophora merlangi.

Bacteria are not normal residents of the gut caeca of Diclidophora merlangi and are found in the gut lumen only as a result of contamination of the culture medium. Mycoplasma-like organisms have been found in the cytoplasm of gland cells associated with the anterior alimentary tract of the worm. Their occurrence is infrequent and does not involve cytoplasmic damage in the gland cell. Unlike the gut luminal bacteria, the mycoplasmas can be found in fresh worms and in worms kept in culture media containing antibiotics.     

Metazoan parasites of the thumb grenadier Nezumia pulchella, from the south-eastern Pacific, off Chile, and their use for discrimination of host populations

The parasite communities of Nezumia pulchella across its geographical range in the south-eastern Pacific were described, from 217 fish captured from four localities in northern and central Chile (24° S to 33° S). Five ectoparasites and 13 endoparasites were recorded and the highest prevalence and intensity of infection was found for the copepods Jusheyhoea macrura and Clavella sp. 1, for the monogenean Diclidophora sp. and for the larval acanthocephalan Corynosoma australe . Parasite species richness decreased with latitude. Multivariate discriminant analysis and correspondence analysis supported the use of parasites of N. pulchella to discriminate populations of this host, suggesting the existence of three well-defined host populations in the geographical range examined. Jusheyhoea macrura , C. australe , Lophoura sp., Diclidophora sp., Capillaria sp. and Proleptus sp. were the most important species for discriminant analysis.     

Parasites as biological markers: evolutionary relationships in the heterospecific combination of helminths (monogeneans) and teleosts (Gadidae)

Analysis of the genetic structure (11 loci) of helminth populations (Monogenea, Diclidophora ), parasites of two teleost species (Gadidae, Trisopterus luscus and T. minutus minulus ) which are sympatric in the Atlantic, revealed the existence of two species which were specific to each of the two hosts. A strong genetic similitude was found between one of these species ( Diclidophora luscae ), a parasite of T. luscus and a monogenean population parasitizing a third Gadidae ( Trisopterus minutus capelanus ) in the Mediterranean. These results led to a re-examinination of the evolutionary systematics of the three host taxa of the genus Trisopterus. Genetic analysis showed differences between the two subspecies T. minutus minutus (Atlantic) and T. minutus capelanus (Mediterranean) at eight of the 16 loci studied. However, there was no significant genetic divergence between T. luscus and T.m. capelanus. A new phyletic structure in the genus Trisopterus is proposed and the evolutionary trends within the Gadidae/Monogenea system are discussed.     

A comparative study of the structure of the oncomiracidia of the monogenean gill parasites Diclidophora merlangi,D. luscae and D. denticulata

The structure of the oncomiracidia of gill parasites Diclidophora merlangi, D. luscae and D. denticulata is described. The three larvae differ in body length and in the size and arrangement of the hooks but the glandular components and excretory systems are similar. There is some evidence that glandular secretions aid hatching. In newly hatched larvae of D. merlangi marginal hook III is displaced and a pouch of tissue occurs between hooks II and IV. The pouches are presumptive clamp tissue. Many larvae fail to hatch in vitro but form one pair of clamps while within the egg capsule.     

Notes on helminth parasites of the whiting Odontogadus m. merlangus (L.) from the northern Irish Sea

In an examination of 1352 whiting from the Irish Sea 13 helminth species were discovered. One species, Scolex polymorphus Rudolphi, was a new species associated with whiting and 7 other species were new species for whiting from the Northern Irish Sea. The species of the digenean genus Podocotyle found in whiting is probably an ecotype of P. atomon. It was concluded that the bothridial structure of 5. polymorphus cannot be used for diagnostic purposes nor to determine early and late stages of the larvae. The number of Diclidophora merlangi Kuhn (Monogenea) from each monthly sample with eggs in the uterus is directly proportional to temperature, but egg production under experimental conditions was greatest at 6° C. Several theories are proposed to explain these apparently contradictory observations. The life-history of the digenean Stephanostomum pristis Looss, appears to be unusual in that the 2nd intermediate host may be planktonic. The nematode Contra caecum clavatum Rudolphi is found both as larvae and adults but larvae comprise the greater part of the worm population. The discovery of small stage II larvae in the stomach of whiting supports the theory that only one intermediate host is necessary for the development of Contmcaecum . There were significantly more female C. clavatum than male but a 1: 1 sex ratio is demonstrated by the acanthocephalan Echinorhynchus gadi Muller. Early and late forms of the plerocercoid of Grillotia erinaceus Van Beneden are identified. The early form occurred predominantly in the young whiting.     

Hatching rhythms in three species of Diclidophora (Monogenea) with observations on host behaviour.

Eggs of three species of Diclidophora were incubated in alternating 12 h periods of light and darkness at 13 degrees C. Eggs of D. merlangi collected at Arbroath hatched during the illumination period with most larvae being recovered in the first 4-6 h; some evidence of a seasonal difference in hatching of these eggs was found. Eggs of D. merlangi collected at Plymouth hatched with a peak of larval recovery in the 2 h period before the light came on. Eggs of D. luscae hatched over 'dusk' while those of D. denticulata hatched after the light was switched off. Neither mechanical disturbance nor the proximity of host tissue caused hatching in D. merlangi or D. luscae. Observations on the behaviour of the host fishes suggest that the hatching rhythms are adapted to specific host behaviour patterns.     

The surface topography of a monogenean, Diclidophora merlangi revealed by scanning electron microscopy

The body surface of adult Diclidophora merlangi is characterized by an annular array of irregularly-shaped ridges, with the intervening troughs of tegument invested with microvilli. The microvilli measure approximately 0.5 micrometer in length and 0.06 micrometer in diameter and at maximum density (10.8/micrometer 2) increase the body surface area by a factor of two. On the anterio-dorsal surface of each peduncle the ridge-like structures consolidate as a distinct area of ornamentaltion some 100 micrometer in diameter. A frontal pit opens just inside the mouth and is thought to provide the outlet for the buccal gland secretions. The tegument surrounding the gonopore and paired excretory pores is unmodified in morphology. Presumed sensory endings are of at least two types: (1) uniciliated structures, projecting from a pit or supported by a collar of tegument, and distributed either singly over the general body surface and in the buccal cavity, or in groups around the mouth; and (2) large numbers of non-ciliated papillae localized on the opisthaptor. A number of these papillae occur on a wart-like outgrowth of tegument positioned on the ventral surface of each peduncle and have obvious significance in contact communications.     

Diclidophora merlangi: Sloughing and renewal of hematin cells

Electron microscopy and section autoradiography have been used in an attempt to find evidence of sloughing and renewal of hematin (digestive) cells in the gut of Diclidophora merlangi. Hematin cells are connected by septate desmosomes to a polymorphic, syncytial connecting tissue which supports and protects each cell from stresses imposed on the gut by body movements. The sloughing of hematin cells occurs only rarely, and evidence of the event is restricted to the occasional finding of a free and relatively undamaged cell in the lumen of the main ceca. The connecting syncytium of the main ceca leading to the foregut is attenuated and, in places, perforated by small pores. Small, undifferentiated cells can be found below the pores, and some of these cells may represent embryonic gut cells. Immature hematin cells, without pigment or Golgi stacks, border the lumen in this region of the gut and are connected to the syncytium by septate desmosomes. Pulse-chase experiments with tritiated thymidine indicate that any renewal of hematin cells takes place a a very low rate.     

Tachykinin immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host the whiting (Merlangius merlangus): radioimmunoassay and chromatographic characterisation using region-specific substance P and neurokinin A antisera

1. Tachykinin immunoreactivity has been quantified and chemically characterised in extracts of the monogenean parasite, Diclidophora merlangi and its fish host, Merlangius merlangus, by means of four tachykinin radioimmunoassays interfaced with gel permeation chromatography and reverse-phase HPLC. 2. Of the two tachykinins identified in parasite tissue, one was SP-like and the other was NKA-like, although neither was identical to previously identified tachykinins. 3. Three tachykinins were identified in extracts of whiting GI tract, one of which was a neuropeptide and also occurred in whiting brain. 4. The parasite and fish tachykinins had different molecular weights and elution profiles in HPLC analyses, and were therefore chemically distinct.     

Diclidophora merlangi and Entobdella soleae: egg production and oxygen consumption at different oxygen partial pressures

The rates of respiration and of egg production of the monogenean trematodes Diclidophora merlangi and Entobdella soleae were compared at different oxygen partial pressures. In D. merlangi the respiratory rate declined sharply as the oxygen pressure in the water fell and egg production almost ceased at pO₂s little below air saturation. Diclidophora lives on the gills of a pelagic fish and the likelihood that the parasite normally has air saturated water passing over it is discussed. Both respiratory rate and egg production in E. soleae were almost independent of ambient pO₂. Entobdella lives on the undersurface of a flat fish, which spends part of its time buried in sandy mud.     

Diclidophora merlangi (Monogenea: Diclidophoridae) on Atlantic cod, Gadus morhua

Diclidophora merlangi (Kuhn, in Nordmann, 1832), as species specific to whiting, Merlangius merlangus (Linnaeus, 1758), is reported and described for the first time on the gills of Atlantic cod Gadus morhua (Linnaeus, 1758). Of the about 1,200 cod examined in this article, only 2 specimens of D. merlangi occurred on 2 fish, suggesting that they represented accidental infections. The 2 specimens showed specific traits of D. merlangi, but their size was considerably smaller than that of D. merlangi on whiting. Principal-component analyses showed that the morphology of the specimens on cod was more similar to that of D. merlangi than those of other congeneric species from the North Atlantic, additionally supporting their assignment to D. merlangi. Quantitative data documenting the potential reproductive consequences of D. merlangi occurring on cod is also provided. The testes and germaria of the specimens on cod were noticeably smaller than those of D. merlangi on whiting, but the number of testes was similar and spermatozoa were observed in the sperm duct. By contrast, the aspect and smaller size of the oocytes suggested that D. merlangi on cod could not produce viable ova, although 1 specimen exhibited an egg with normal sized and shaped capsule.     

Ultrastructure of the male accessory ducts and prostate gland of Diclidophora merlangi (Monogenoidea)

The vas deferens, seminal vesicle, penis and common genital atrium of the monogenean, Diclidophora merlangi are lined by a very flat, lamellate epithelium. The structure is apparently syncytical, although nuclei or perikaryons have not been observed. The epithelium extends to just inside the gonopore where a septate desmosome marks the union with body tegument. There is minor regional variation in structure. The terminal portion of the seminal vesicle and the penis lumen are lined in part by the luminal cytoplasm of the prostate gland which surrounds this part of the reproductive tract. The prostate gland cells are synthetically active and produce a characteristic secretory body that is released either singly by exocytosis, involving membrane fusion, or in bulk via apocrine secretion. The secretion is acidophilic, PAS-positive and reactive for protein. The penis is sucker-like in structure and armed with a ring of 16 genital hooklets. Cilia have not been observed in any part of the male reproductive tract, and sense receptors are not apparent in the tegument surrounding the gonopore.     

Ultrastructure of the anterior alimentary tract of a monogenean, Diclidophora merlangi

The anterior alimentary tract of Diclidophora merlangi is composed of a complex series of morphologically distinct epithelia interconnected by septate desmosomes and penetrated by the openings of numerous unicellular glands. The mouth and buccal cavity are lined by an infolding of modified body tegument, distinguished by uniciliate sense receptors, buccal gland openings, and in the buccal region by a dense, spiny appearance. The prepharynx is covered by an irregularly folded epithelium and, for part of its length, by the luminal cytoplasm of the prepharyngeal gland cells. The epithelium is syncytial and pleiomorphic, and regional variation in structure is common. A separate epithelium invests the lips of the pharynx and its free surface is greatly amplified by numerous, dense lamellae of varying dimensions. The lip epithelium is continuous with cytoplasmic processes of cells located external to the pharynx. A further, distinct epithelium borders the pharynx lumen and is composed of discrete cytoplasmic units connected by short septate desmosomes. The oesophagus is lined by a modified caecal epithelium, lacking haematin cells, and, in places, is perforated by the openings of oesophageal gland cells; it is continuous with the syncytial connecting tissue of the gut caeca.     

Immunocytochemical demonstration of neuropeptides in the fish-gill parasite, Diclidophora merlangi (Monogenoidea)

Using the indirect immunofluorescence technique, immunoreactivity (IR) to three mammalian and one invertebrate regulatory peptide has been demonstrated in the nervous system of the monogenean gill parasite Diclidophora merlangi. IR to pancreatic polypeptide (PP), peptide tyrosine tyrosine (PYY) and FMRFamide was evident throughout central and peripheral nervous tissues, whereas vasoactive intestinal polypeptide (VIP)-IR was confined to a portion of the longitudinal ventral nerve cords. Staining patterns revealed the orthogonal arrangement of the nervous system consisting of paired cerebral ganglia, connecting post-pharyngeal commissure, three pairs of longitudinal nerve cords and associated neurones. PP-IR, PYY-IR and FMRFamide-IR were intense throughout the central nervous system of the worm. A small plexus of nerve fibres and somata in each peduncle was immunoreactive for FMRFamide and provided innervation to each of the eight posterior clamps. In the peripheral nervous system, PP-IR, PYY-IR and FMRFamide-IR occurred in an extensive nerve-net with fine, possibly sensory nerve endings in the tegument. PP-IR was also present in nerve fibres in the walls of the ootype, seminal vesicle and uterus. PYY- and FMRFamide-IRs, while evident in nerve fibres of the ootype wall, were also present in a distinct population of cells that encircles the ootype, and which are linked to it by fine cytoplasmic connectives. The majority of these somata were bipolar or multipolar. PYY-IR and FMRFamide-IR were also associated with nerve fibres and bipolar cells in the wall of the vitelline reservoir. Regulatory peptides would appear to play an integral role in neuronal functioning and egg development in D. merlangi.     

Taxonomy of monogeneans of deep sea fishes in southeastern Australia

The following monogeneans from deepwater fish in southeastern Australia are described, based on a survey of 1,563 fish (66 or 67 species, 35 families, 15 orders): Reimericotyle ceratoscopeli from Myctophum phengodes, M. hygomi, Hygophum hygomi and Ceratoscopelus warmingii; Diclidophora tubiformis n. sp. from Coryphaenoides serrulatus and C. subserrulatus; Diclidophora sp. from Lepidorhynchus denticulatus; Polycliphora nezumiae from Coryphaenoides serrulatus; Paracyclocotyla sp. from Lepidion microcephalus; juvenile Paracyclocotyla sp. from Hoplostethus atlanticus; Polyipnicola hygophi from Hygophum hygomi, Notoscopelus resplendens, Electrona risso and Myctophum phengodes; Diclidophoropsis sp. from Nezumia sp.; Eurysorchis manteri from Hyperoglyphe sp.; Heteraxinoides sp. from Synagrops japonicus; Megalocotyle helicoleni from Helicolenis papillosus. The following species are recorded but not described: Allocotylophora polyprionum (Diclidophoroidea), four unidentified species of the Diclidophoroidea from Diastobranchus capensis, both Hoplostethus atlanticus and H. intermedius, Chlorophthalmus sp. and Synagrops japonicus, respectively, one species of the Capsaloidea from Enoplosus armatus, one species of the Capsalidae from Lepidotrigla argus, one species of the Dactylogyrinae from Atypichthys strigatus, and one species of the Ancyrocephalinae from Chlorophthalmus nigripinnis.     

Segregation of SE Pacific and SW Atlantic southern blue whiting stocks: integrating evidence from complementary otolith microchemistry and parasite assemblage approaches

Southern blue whiting Micromesistius australis support one of the largest industrial fisheries in South America. Two main spawning/nursery grounds are known: one in the SW Atlantic Ocean (SWA), southwest from the Falkland (Malvinas) Islands; and other in the SE Pacific Ocean (SEP), south from the Taitao Peninsula. Juveniles originating from both grounds are believed to mix during migration and/or in feeding areas in the Scotia Sea. Previous efforts to distinguish stocks in this area have yielded contradictory results between genetics and otolith microchemical analyses. In the present work we revisited the null hypothesis of a single stock occurring in the broader SWA-SEP region by comparing and integrating results from different approaches: trace metals (Ca, Sr, Ba, Mg, Mn) and stable isotopes (δ¹³C, δ¹⁸O) in otolith cores, and parasite assemblage compositions in adults from SWA and SEP spawning grounds. We found significant differences in Sr:Ca, δ¹³C and δ¹⁸O mean ratios between spawning grounds. The best trace element discriminant model classified 83% of the samples. Each stable isotope discriminated >90% of the samples, while combining them into a bivariate discriminant model led to 100% classification success. Higher δ¹⁸O levels in the SWA samples agreed with lower mean temperature and higher ambient δ¹⁸O levels in that area. Parasite assemblage compositions also showed significant differences between grounds regarding the prevalence of Chondracanthus, Contracaecum, Hepatoxylon and Grillotia and the abundance of Diclidophora, Anisakis, Contracaecum, Hysterothylacium and Hepatoxylon. Parasite-based discriminant models supported 90–100% correct assignment of samples to capture location. Although preliminary due to limited sampling coverage, our results support the existence of at least two ecologically distinct sub-populations of southern blue whiting in South America. The joint use of otolith microchemistry and parasitological techniques showed to be a promising way to test hypotheses concerning ecological stocks in marine fishes.     

Revision of the genus Diclidophora Krøyer, 1838 (Monogenea: Diclidophoridae), with the proposal of Macrouridophora n. g.

The present study re-examines the detailed morphology of the type-species, Diclidophora merlangi (Kuhn, in Nordmann, 1832) Krøyer, 1838, and other Diclidophora species parasitic on gadid fishes: D. denticulata (Olsson, 1876) Price, 1943, D. esmarkii (Th. Scott, 1901) Sproston, 1946, D. luscae (van Beneden & Hesse, 1863) Price, 1943, D. minor (Olsson, 1868) Sproston, 1946, D. palmata (Leuckart, 1830) Diesing, 1850, D. phycidis (Parona & Perugia, 1889) Sproston, 1946, D. pollachii (van Beneden & Hesse, 1863) Price, 1943 and the recently described D. micromesisti Suriano & Martorelli, 1984. An amended generic diagnosis of Diclidophora Krøyer, 1838 (synonym Diclidophora Diesing, 1850) is provided, which includes the presence of a prostatic vesicle in the terminal male genitalia and the distal fusion of the median and peripheral sclerites, a₁ and c₁ in the clamp anterior jaw. Macrouridophora n. g. is herein proposed for species previously considered in Diclidophora, which are parasitic on macrourid and morid fishes. The clamp morphology in Macrouridophora n. g. has distinct lamellate extension attachments to peripheral sclerites c₁ and the distal portion of d₁, with no distal fusion between a₁ and c₁ in the anterior jaw. Macrouridophora macruri (Brinkmann, 1942) n. comb. is chosen as the type-species. Nine other species are herein transferred to Macrouridophora n. g.: M. coelorhynchi (Robinson, 1961) n. comb., M. lotella (Machida, 1972) n. comb., M. nezumiae (Munroe, Campbell & Zwerner, 1981) n. comb. and M. tubiformis (Rohde & Williams, 1987) n. comb. are redescribed, based on the re-examination of type or voucher specimens. Macrouridophora attenuata (Mamaev & Zubtschenko, 1979) n. comb., M. caudata (Mamaev & Zubtschenko, 1984) n. comb., M. papilio (Mamaev & Avdeev, 1981) n. comb., M. paracoelorhynchi (Mamaev & Paruchin, 1979) n. comb. and M. physiculi (Mamaev & Avdeev, 1981) n. comb. have adequately described haptoral clamps in the literature. The clamp morphology in Macrouridophora sp. from Lepidorhynchus denticulatus in Australia is also considered. Diclidophora whitsonii Suriano & Martorelli, 1984 is herein transferred to the genus Macruricotyle Mamaev & Ljadov, 1975, as M. whitsonii (Suriano & Martorelli, 1984) n. comb. D. embiotocae Hanson, 1979 is herein considered a species incertae sedis. D. caudospina Khan & Karyakarte, 1983 and D. paddiforma Deo & Karyakarte, 1979 are herein considered species inquirendae. D. aglandulosa Deo, 1977, D. glandulosa Das, 1972, D. minuta Das, 1972 and D. spindale Deo, 1977 are formally dismissed as nomina nuda. The systematic position of Diclidophora Krøyer, 1838 and Macrouridophora n. g. in the subfamily Diclidophorinae Cerfontaine, 1895 (sensu Mamaev, 1976) is discussed.