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Microthrix pattern of Pseudogilquinia thomasi (Palm, 2000) (Cestoda: Trypanorhyncha) and a review of surface ultrastructure within the family Lacistorhynchidae Guiart, 1927

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Abstract

The microthrix pattern of larvae of Pseudogilquinia thomasi (Palm, 2000) is described for the first time using scanning electron microscopy. The surface ultrastructure of this species consists of three main forms of microtriches: papilliform filitriches, acicular filitriches and quadridigitate to octadigitate palmate spinitriches. The bothria are covered with palmate spinitriches interspersed on some parts with papilliform filitriches. Palmate spinitriches with papilliform, acicular and capilliform filitriches adorn the pars vaginalis and at the anterior part of the pars bulbosa, there is a transition zone in which the palmate spinitriches are replaced by papilliform to acicular filitriches towards the end of the scolex. ANOVA tests with Duncan's post hoc analyses revealed that there are significant differences in the length of spinitriches and their prongs, whether on the surfaces of the bothria or on the surfaces of the scolex peduncle. Callitetrarhynchus gracilis Pintner, 1931 is the second lacistorhynchid species for which surfaces of the segments were examined and the occurrence of large structures called scutes are reported for the first time from this species. There were also significant differences in the base length as well as height of the scutes in different parts of the strobila. In addition to describing the surface ultrastructures of the two lacistorhynchid species, all the available information on the microtriches within the family Lacistorhynchidae is reviewed herein and generic diagnoses related to microtriches are amended. J. Morphol., 2015. © 2015 Wiley Periodicals, Inc.

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... Scanning electron microscopy (SEM) reveals different kinds of microtriches across the entire surface of the tegument of the different groups of cestodes (Chervy, 2009;Faliex et al., 2000;Caira et al., 1999). There are different forms of microtriches in the different groups of trypanorhynchs, such as capilliform, papilliform, palmate, filiform, and others ( Figure 2) (Whittaker, 1985;Palm, 2008;Caira et al., 2010;Menoret and Ivanov, 2015;Haseli et al., 2016). ...
... Most faunistic studies of trypanorhynchs from the northwestern Indian Ocean have been carried out in the northern Persian Gulf and in part in Iranian coastal waters of the Gulf of Oman (Haseli, 2013;Haseli et al., 2010Haseli et al., , 2011Haseli et al., , 2016Haghighi-Pour Choukami & Haseli, 2016;Haseli & Malekpour Fard, 2017;Haseli & Palm, 2015;Salmani & Haseli, 2017;Shafiei & Haseli, 2019). Likewise, Kardousha (1991, 1999), El Naffar et al. (1992, Saif et al. (1994), and Hassan et al. (2002) reported larval trypanorhynchs from bony fishes in the southern Persian Gulf. ...
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... Palm et al., 1998Palm et al., , 2009, the microtriches of the bothrial pits as well as the bothrial grooves in the otobothrioids have been rarely compared to those of the bothrial grooves in the lacistorhynchoids (see Palm, 2004). Of the 17 otobothrioid species, the surface ultrastructure of which has been studied (Palm, 1995(Palm, , 2000(Palm, , 2004Beveridge & Justine, 2007;Schaeffner & Beveridge, 2013a, b), the chelate spinitriches covering the bothrial pits in O. elenae n. g., n. sp., Proemotobothrium southwelli, Otobothrium australe Palm, 2004, Otobothrium mugilis Hiscock, 1954, Otobothrium sp. 1 sensu Beveridge, 2013 andPoeciloacanthum oweni Palm, 1995 also adorn the bothrial grooves of the lacistorhynchid species Grillotia amblyrhynchos Campbell & Beveridge, 1993, Callitetrarhynchus speciosus (Linton, 1897, Callitetrarhynchus gracilis Pintner, 1931, Floriceps minacanthus Campbell & Beveridge, 1987 and Bombycirhynchus sphyraenaicum (Pintner, 1930) (see Haseli et al., 2016). In addition, the bifid spinitriches covering the bothrial groove in O. elenae n. g., n. sp. as well as the bothrial pits in Symbothriorhynchus tigaminacantha and Otobothrium penetrans also adorn the bothrial grooves of the lacistorhynchoid species Pseudogilquinia pillersi (Southwell, 1929) Palm, 2004). ...
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Specimens of Floriceps minacanthus Campbell & Beveridge, 1987 are reported from Carcharhinus melanopterus (Quoy & Gaimard, 1824) taken in the waters surrounding the island of Kirimati in the Republic of Kiribati in the Central Pacific Ocean. This represents a new host and a new locality record. The description of this species is expanded to include the presence of an ovary which is bilobed in cross section and a hermaphroditic duct. The surface features were examined by scanning electron microscopy. With the exception of the lateral margins of the bothridia and the apical region of the scolex, the scolex was found to be covered with palmate microtriches interspersed with filiform microtriches. The palmate microtriches varied in number of digitiform extensions depending on location. Elongate, bifid microtriches were present in the transition zone between the proximal and distal surfaces along the lateral margins of the bothridia. The apical region of the scolex was covered with filiform microtriches. The surface of the anterior margin of the strobila was covered with broad, flattened scale-like structures. The pattern of microthrix distribution was repeated for each of the bothridia of an individual, and this pattern was intraspecifically invariable. Comparison of our results with those from the seven other trypanorhynch species examined by previous authors with SEM indicates that there is much interspecific variability in both the morphology of microtriches present as well as their location on the scolex. This, coupled with the lack of intraspecific variability, confirms that these structures are systematically informative.
Article
Abstract A new species of Grillotia was found from teleosts and elasmobranchs along the Patagonian shelf off Argentina. Grillotia patagonica n. sp. is described from plerocerci recovered from gadiform (Moridae) and perciform fish (Cheilodactylidae, Bovichtidae, and Nototheniidae), and adults from the smallthorn sand skate Psammobatis rudis (Rajiformes, Rajidae). Grillotia patagonica most closely resembles species in the G. erinaceus species complex (viz., G. borealis, G. brayi, G. dollfusi, G. erinaceus, and G. musculara) in having 4 hooks per principal row and 2, or more, intercalary rows in the metabasal region, a band of hooks on the external surface of the tentacle, numerous proglottids, a hermaphroditic sac, internal and external seminal vesicles, uterine pore, and attachment of the retractor muscle in the mid region of the tentacular bulb. It is unique among all valid species in the genus by having the hooks on the 1st row reduced and of a different shape from the rest of the metabasal rows. Despite the diversity of elasmobranchs that are available as definitive hosts for species in Grillotia, most species (10/14) are oioxenous or mesostenoxenous. The specificity for the last intermediate host is variable among species of Grillotia, with most plerocerci being oioxenous (5/15) or euryxenous (8/15). Host specificity is higher for the adult stage in the definitive host (mean HSs = 4.07) than for the plerocerci (mean HSs = 7.30). All the species with oioxenous specificity (either larvae or adults) have limited geographic distributions. Some previous records of species of Grillotia from fishes caught off Argentina require reconsideration, i.e., G. erinaceus, G. minuta (reported as G. bothridiopunctata) and G. borealis. An updated host-parasite checklist for the valid species of Grillotia is also presented, along with new host records for G. carvajalregorum.
Article
A total of 299 fish belonging to ten teleost species were studied in Iranian waters at the north-eastern coast of the Persian Gulf for larval trypanorhynch cestode infection. The following trypanorhynch species were identified: Callitetrarhynchus gracilis Pintner, 1931, Pseudogilquinia thomasi (Palm, 2000), Pterobothrium lesteri Campbell and Beveridge, 1996 and Pseudolacistorhynchus shipleyi (Southwell, 1929). The most abundant parasite was C. gracilis which was isolated from seven teleost species. The highest prevalence (62.9%) and dominance (0.98) were demonstrated for P. thomasi with a maximum intensity of 22 in Indian halibut Psettodes erumei. Collections of P. lesteri and P. shipleyi from the Persian Gulf represent new locality records, thus extending the known range of distribution for both species. Four new host records are established. The recorded combination of trypanorhynch species and the established host range correspond to other regions, such as off the Brazilian coast. In terms of species distribution, the north-western part of the Indian Ocean, together with the Gulf of Bengal and the Indonesian archipelago, share the same species, resulting from connected water bodies. All trypanorhynch species were isolated from the body cavity, except for P. thomasi which was recorded from the musculature of P. erumei. Relatively high intensities of infection in P. erumei may be of public health concern in the region, necessitating the consumption of well-cooked fish products.
Article
Christianella Guiart, 1931 (Cestoda: Trypanorhyncha) is redefined as a subgenus of Grillotia Guiart, 1927 based on the type-species, G. (C.) minuta (van Beneden, 1849), from the elasmobranch Squatina squatina (Linnaeus). Grillotia smarisgora (Wagener, 1854) is treated as a synonym of G. (C.) minuta, as are G. angeli Dollfus, 1969 and G. bothridiopunctata Dollfus, 1969. Other species included in the subgenus are G. (C.) carvajalregorum Menoret & Ivanov, 2009 (formerly Progrillotia dollfusi Carvajal & Rego, 1983), G. (C.) australis Beveridge & Campbell, 2001, G. (C.) longispinis (Linton, 1890) n. comb. (formerly Rhynchobothrium longispine Linton, 1890) and G. (C.) yuniariae Palm, 2004. The subgenus is similar to Grillotia Guiart, 1927 (sensu stricto), having two bothria and an atypical heteroacanthous armature, but differs in having a single row of intercalary hooks, fewer, elongate segments with testes often in longitudinal columns, a distinctive basal armature, an internal seminal vesicle which extends beyond the cirrus or hermaphroditic sac and no uterine pore. The adults of three species are known, all parasitising members of Squatina Duméril.
Article
Terminology for microtriches, the surface features both unique to and ubiquitous among cestodes, is standardised based on discussions that occurred at the International Workshops on Cestode Systematics in Storrs, Connecticut, USA in 2002, in Ceské Budejovice, Czech Republic in 2005 and in Smolenice, Slovakia in 2008. The following terms were endorsed for the components of individual microtriches: The distal, electron-dense portion is the cap, the proximal more electron-lucent region is the base. These two elements are separated from one another by the baseplate. The base is composed of, among other elements, microfilaments. The cap is composed of cap tubules. The electron-lucent central portion of the base is referred to as the core. The core may be surrounded by an electron-dense tunic. The entire microthrix is bounded by a plasma membrane, the external layer of which is referred to as the glycocalyx. Two distinct sizes of microtriches are recognised: those < or = 200 nm in basal width, termed filitriches, and those >200 nm in basal width, termed spinitriches. Filitriches are considered to occur in three lengths: papilliform (< or = 2 times as long as wide), acicular (2-6 times as long as wide), and capilliform (>6 times as long as wide). In instances in which filitriches appear to be doubled at their base, the modifier duplicated is used. Spinitriches are much more variable in form. At present a total of 25 spinithrix shapes are recognised. These consist of 13 in which the width greatly exceeds the thickness (i.e., bifid, bifurcate, cordate, gladiate, hamulate, lanceolate, lineate, lingulate, palmate, pectinate, spathulate, trifid, and trifurcate), and 12 in which width and thickness are approximately equal (i.e., chelate, clavate, columnar, coniform, costate, cyrillionate, hastate, rostrate, scolopate, stellate, trullate, and uncinate). Spiniform microtriches can bear marginal (serrate) and/or dorsoventral (gongylate) elaborations; they can also bear apical features (aristate). The latter two modifiers should be used only if the features are present. The terminology to describe the overall form of a spinithrix should be used in the following order: tip, margins, shape. Each type of microthrix variation is defined and illustrated with one or more scanning electron micrographs. An indication of the taxa in which each of the microthrix forms is found is also provided.
Article
The tapeworm "cuticle" is, in reality, a cellular syncytium, referred to in the recent literature as a tegument. Lacking a gut, tapeworms utilize the tegment alone for chemical interchange with the host. Attendant to this function is a brush border containing a number of transport mechanisms and hydrolytic enzymes. The external limiting membrane is coated with a layer of carbohydrate-rich polyelectrolytes, viz. a glycocalyx. This structure serves as a binding surface for inorganic ions and higher molecular weight organic compounds, including host enzymes. Certain of the latter retain activity, and may thereby contribute to contact-digestive functions at the surface of the worm. Others are bound in a catalytically-inactive configuration, which may serve to protect the parasite from digestion. Intrinsic enzymes of the tegument membrane surface include phosphohydrolases and a ribonuclease; the hydrolysis products of these activities interact with proximal transport loci and are thereby absorbed. Thus, the tapeworm tegument includes a digestive-absorptive-protective surface, whose functions involve the interaction of both parasite and host components within the structural framework of a membrane-defined interface.
Article
Nematodes, trematodes, cestodes, and acanthocephalans each have become adapted in different ways to the microenvironment of the vertebrate intestine. Life in this specialized habitat affords parasites a reliable source of nutrients, a relatively homeostatic environment, and protection from predators but, in exchange for these advantages, presents the special challenges of exposure to digestive enzymes, normal peristalsis, and host immune response to infection. Logically, the surface of the parasite should be the first part of the organism to encounter such challenges, and, for this reason, any response or reaction by the parasite is expected to be manifested at the parasite-host interface. Morphological adaptations of intestinal helminths to their microenvironment include modification of the tegumental surface that affords protection and increases absorptive surface area, development of specialized attachment organs, and, in some cases, complete loss of their own internal digestive system. Representative examples of such adaptations by helminths are described and discussed in terms of the parasite's nutritional requirements, site selection, and host specificity, and the possibility is suggested that some helminths may have adapted in ways that exploit host defensive mechanisms for their own benefit.
Article
Scanning electron micrographs of the tegument of three species of Hymenolepis have revealed polymorphic microtriches. In H. diminuta ontogenetic allometric growth results in mature/early gravid segments having two distinct populations of posteriorly-oriented microtriches: one short (ca. 1µ), tubular, with conical tips; another long (ca. 5µ), flattened, with spatulate tips. H. nana's microtriches are polymorphic and primarily oriented at right angles to its tegument. In H. microstoma microtrichial dimorphism is apparent in the neck and immature strobilar region. The large microtriches in the neck region of this species point in many directions, but most assume a posterior orientation as the segments mature. All three species exhibit a decreased microtrichial density down the length of the strobila and morphological changes in the tegumental surface of the gravid segments. Such changes involve surface sculpturing in the anterior two-thirds of the segment accompanied by loss of all microtriches and erosion of folds in the posterior third. Relatively small (ca. 3x) increase in surface tegumental area due to the microtriches suggests that they do not play an important role in nutrient absorption. The larger microtriches may play a locomotory role in site-selection and intra-luminal migrations of these worms.
Article
The teguments of adult E. granulosus, T. hydatigena, and T. pisiformis were examined with the electron microscope. These species have teguments consisting of a cytoplasmic modification (the distal cytoplasm) of cells (perinuclear cytoplasm) lying in the parenchyma. Projections cover the surface of the tegument. The distal cytoplasm is filled with vesicular inclusions. Mitochondria are confined to the basal portion of the distal cytoplasm. Slender extensions provide cytoplasmic continuity between the distal and perinuclear cytoplasm. The distal cytoplasm rests on a fibrous zone which is continuous with the extracellular spaces in the parenchyma. Fine strands cross this zone to connect the basal membrane of the distal cytoplasm with the muscle bundles. Cells containing glycogen granules are seen in the parenchyma. The tegument is multinucleated in some places. The observations support the view that tapeworm teguments have a syncytial arrangement. Pore canals which penetrate the distal cytoplasm are interpreted as tubular structures and not as cellular boundaries.
Article
Ultrastructural observations on adult Proteocephalus tidswelli revealed a marked microtrichial polymorphism. Structural and dimensional variations of microtriches between different regions of the strobila and scolex, as well as within the same region, were observed. The authors suggest that microtriches are involved in a diversity of functions, and possible functional activities are discussed.
Article
A new trypanorhynch cestode, Grillotia borealis sp. n., is described from the spiral intestines of softnose skates of the genus Bathyraja collected from subarctic waters of the North Pacific Ocean: B. parmifera (Bean) (type host), B. aleutica (Gilbert) and B. interrupta (Gill et Townsend) from the Bering Sea and B. minispinosa Ishiyama et Ishihara and B. sminovi (Soldatov et Pavlenko) from the Sea of Okhotsk off Japan. The new species is distinguished from other species of Grillotia by possession of the following combination of characters: four hooks per principal row, hooks 4(4') distinctly separated from hooks 3(3') of principal row, principal rows separated by 13-15 intercalary hooks in 2-3 rows, hooks 2(2') and 3(3') change in form along their respective files, hooks 1(1') do not change in form along the file, a broad band of microhooks on the external tentacular face, intermediary hooks are lacking, absence of a special basal armature, origin of the retractor muscle near middle of the bulb, average scolex ratio of 1:3:2:0.1, and a hermaphroditic sac. Grillotia borealis consistently favoured the most anterior regions of the spiral intestine. Seventy-one per cent of 21 attached worms occupied the most anterior chamber of the spiral valve and 52 per cent were embedded in the anterior surface of the spiral valve whorls. Factors which may limit the distribution of G. borealis within the spiral intestine of its host are discussed. Statistically significant differences occur in the mucosal morphology of B. aleutica and B. parmifera for villus length, diameter, spatial arrangement and number per unit area along the antero-posterior axis of the spiral intestine.
Article
Two new species of Grillotia are described from elasmobranch and teleost fishes from south-eastern Australia. G. australis n. sp., from the Australian angel shark Squatina australis. Regan, most closely resembles G. smarisgora (Wagener, 1854) and G. angeli Dollfus, 1969, differing from both species in the presence of smaller bulbs, two or occasionally three hooks in each intercalary row in the basal region, reduced to one in the metabasal region compared with four or five hooks in the metabasal region of G. smarisgora and a single hook in G. angeli, and in the limited extent of the band of hooklets on the external surface in the basal region of the tentacle, a region which is covered with hooks in G. smarisgora. Plerocerci of this species were found in the mackerel Trachurus declivis (Jenys) (site not known) from Tasmania. G. pristiophori n. sp., from the saw sharks Pristiophorus cirratus (Latham) and P. nudipinnis Günther, most closely resembles G. spinosissima Dollfus, 1969 in possessing a scolex covered with spiniform microtriches, but differs in having six rather than five hooks in each principal row, no intercalary hooks and by possessing a band of hooklets on the external surface of the tentacle which diminishes distally into a single file, rather than persisting as a band eight to nine files wide. G. pristiophori is the first trypanorhynch to be recorded from saw-sharks.
Article
Members of the trypanorhynch cestode genus Grillotia Guiart, 1927 belonging to the Grillotia erinaceus (van Beneden, 1858) species complex are redescribed. The type-species of the genus, G. erinaceus, is redescribed from Raja spp. in the eastern and western north Atlantic and the Mediterranean. The redescription establishes the presence of: an hermaphroditic sac; internal and external seminal vesicles (but absence of an accessory seminal vesicle); a uterine pore; and the attachment of the retractor muscle in the mid-region of the tentacular bulb. G. pseuderinaceus Dollfus, 1969 and G. recurvispinis Dollfus, 1969 from Raja spp. in the Mediterranean are considered to be synonyms of G. erinaceus, following Palm (2004). G. dollfusi Carvajal, 1971 from R. chilensis Guichenot off Chile is redescribed from the paratypes and features of the terminal genitalia, consistent with those of G. erinaceus, are described for the first time. G. musculara (Hart, 1936) is redescribed from new material collected from the type-host, R. rhina (Jordan & Gilbert), off Nanaimo on the western coast of Canada. The features of the terminal genitalia of G. musculara are similar to those of the G. erinaceus group. The morphological features of G. borealis Keeney & Campbell, 2001 from Bathyraja spp. in the Bering Sea and the Sea of Okhotsk are summarised and illustrations of this species provided. G. brayi n. sp. is described from Amblyraja radiata from the coasts of Iceland and Britain. The new species differs from other members of the complex in lacking modified hooks 1 and 1' at the base of the tentacle (differentiating it from G. erinaceus), a long pars vaginalis (differentiating it from G. dollfusi) and uncinate hooks in the band on the external surface of the tentacle (differentiating it from G. musculara). Brief descriptions are provided of two apparently new species of Grillotia currently represented in collections by single specimens.
Article
The distal bothridial surfaces of adult triloculate onchobothriids are covered with short structures that have been tentatively classified as very short filitriches, but this hypothesis has never been tested. Scanning electron microscopy (SEM) and transmission electron microscopy (TEM) were used to investigate microthrix morphology in the plerocercoid and adult forms of Calliobothrium cf. verticillatum, a triloculate onchobothriid tapeworm from Long Island Sound (Connecticut). Plerocercoids of C. cf. verticillatum were collected from the anterior midgut ceaca of Pagurus pollicaris Say, 1817 (flat-clawed hermit crab), and adults were collected from the spiral intestine of the dusky smooth hound Mustelis canis (Mitchell, 1815). Two plerocercoids and 2 adults were examined using SEM; 2 plerocercoids and 2 adults were examined using TEM. Microthrix distribution and morphology (including measurements of total length, base length, shaft length, and base width) were investigated on all surfaces of the plerocercoid and adult scolex. Slender filitriches and large bladelike spinitriches were observed extending from the tegument of plerocercoid and adult forms. The filitriches were found to have significantly narrower bases than the spinitriches (65-167 nm vs. 466-1,936 nm, respectively). The scolex proper of the plerocercoid and adult forms were found to have filitriches of medium-length and bladelike spinitriches. The distal bothridial surfaces differed dramatically in microthrix morphology between plerocercoid and adult forms; on the distal surfaces of the plerocercoids were long filitriches and bladelike spinitriches. However, the distal surfaces of the adults had short structures (previously hypothesized to be short filitriches) and a few bladelike spinitriches. Serial transverse sections revealed that the short structures on the distal bothridial surfaces of the adults were homologous with filitriches. They included all of the structural components of a filithrix as well as a base width that conformed to the filitriches found on other surfaces. The bothridial margins of the plerocercoid and adult forms had a microthrix pattern similar to that seen on the proximal bothridial surfaces except that the filitriches on the margins were significantly longer than those found anywhere else on the bothridia. The most dramatic difference between the plerocercoid and adult forms occurred on the distal bothridial surfaces, where the filitriches of the adult cestodes were significantly shorter and narrower, and the spinitriches were almost entirely lacking.
Article
Two species of Orygmatobothrium were found inhabiting triakid sharks collected from the coast of Buenos Aires Province, Argentina. Orygmatobothrium schmittii from Mustelus schmitti is redescribed, including new information on the microtrich pattern. Orygmatobothrium juani n. sp. from Mustelus fasciatus can be distinguished from all other species in the genus using the following combination of characters: worm length, number of proglottids, number of testes, testes distribution, size of eggs, ornamented egg shell, shape of bothridial cleft at level of the marginal accessory sucker, and the extension of vitelline follicles. Species in Orygmatobothrium share a common microtrich pattern with the distal bothridial surface covered with maisiform microtriches interspersed with filiform microtriches, a proximal bothridial surface covered with trifid microtriches, with a medial projection conspicuously larger than the lateral basal projections interspersed with filiform microtriches, an inner and outer surface of the accessory sucker and glandulomuscular organ covered with short filiform microtriches, the scolex proper and cephalic peduncle surface covered with bladelike microtriches, and the germinative zone and entire strobila covered with scutes formed by densely packed filiform microtriches. This general configuration is basically similar to the microtrich pattern described in species of Orectolobicestus and Paraorygmatobothrium.
De quelques cestodes tétrarhynques (Hétéracanthes et Pécilacanthes) récoltés chez des poisons de la Mediterraneé
  • Dollfus
Grillotia epinepheli sp. n.(Cestoda: Trypanorhyncha) plerocerci from the teleost, Epinephelus guaza, in Sardinia, Italy
  • Scholz T
The physiology of tapeworms, correlated to structures seen with the electron microscope
  • Rothman AH