Leslie A. Chisholm

A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg, 1879 (Monogenea)

The Monocotylidae Taschenberg, 1879 is revised based on a cladistic analysis of relationships between the constituent species and genera. The monophyly of the family is supported by three apomorphic character states: division of the haptor into one central and eight peripheral loculi; the ovary looping the right intestinal caecum; and tetrahedral eggs. The family is divided into six subfamilies: Calicotylinae Monticelli, 1903 (comprising Calicotyle Diesing, 1850, Dictyocotyle Nybelin, 1941); Dasybatotreminae Bychowsky, 1957 (comprising Anoplocotyloides Young, 1967, Dasybatotrema Price, 1938, Timofeevia n. g., Troglocephalus Young, 1967); Decacotylinae n. subfam. (comprising Decacotyle Young, 1967, Papillicotyle Young, 1967); Heterocotylinae n. subfam. (comprising Heterocotyle Scott, 1904, Neoheterocotyle Hargis, 1955, Nonacotyle Ogawa, 1991, Potamotrygonocotyle Mayes, Brooks & Thorson, 1981, Spinuris Doran, 1953); Merizocotylinae Johnston & Tiegs, 1922 (comprising Cathariotrema Johnston & Tiegs, 1922, Empruthotrema Johnston & Tiegs, 1922, Merizocotyle Cerfontaine, 1894, Squalotrema Kearn & Green, 1983, Triloculotrema Kearn, 1993); and Monocotylinae Taschenberg, 1879 (comprising Clemacotyle Young, 1967, Dendromonocotyle Hargis, 1955, Monocotyle Taschenberg, 1878). The Dendromonocotylinae Hargis, 1955 is removed from subfamilial status and the two genera previously assigned to the subfamily are reassigned to the Monocotylinae. Timofeevia is proposed for Timofeevia rajae (Timofeeva, 1983) n. comb. (formerly Dasybatotrema rajae). Mycteronastes Kearn & Beverley-Burton, 1990 and Thaumatocotyle Scott, 1904 are synonymised with Merizocotyle. Gymnocalicotyle Nybelin, 1941 is not considered a distinct taxon. Revised diagnoses and keys for subfamilies and genera of the Monocotylidae are provided.

The larvae of Monogenea (Platyhelminthes)

Abstract There has been no comprehensive review of the infective larval stage (oncomiracidium) in the direct life-cycle of monogeneans since Llewellyn (1963, 1968). In the last 30 years, knowledge of the general anatomy and morphology of oncomiracidia has increased significantly as has information on swimming behaviour and egg-hatching strategies that may enhance chances of host infection. Nevertheless, oncomiracidia are known for only a small proportion of monogenean species described. This review consolidates established, and summarizes new, knowledge since Llewellyns work and integrates light- and electron-microscopy studies including unpublished data. Currently there is considerable debate, fuelled largely by phylogenetic studies using molecular techniques, about whether or not the class Monogenea (comprising subclasses Monopisthocotylea and Polyopistho-cotylea) is monophyletic. This challenges established views that Monopisthocotylea and Polyopisthocotylea form a single clade based on two larval characters: two pairs of rhabdomeric eyes; three bands of ciliated cells. In an attempt to reveal further synapomorphies for the entire Monogenea (or provide evidence against its monophyly) or possibly for the Monopisthocotylea and Polyopisthocotylea only, we review the following larval features: haptoral sclerites; ciliated cells; epidermis; terminal globule; gland, proto-nephridial and nervous systems; sense organs; digestive tract; parenchyma; and behaviour. Conclusions are equivocal but indicate that further larval studies, especially ultrastructural, are necessary to assess: to presence or absence of ‘false’ vertical rootlets of epidermal cilia; tapering epidermal cilia; the protonephridial system; the presence or absence of a terminal globule; glands and their secretions; and the embryology and chemical composition of haptoral sclerites. Future integration of light- and electron-microscopy studies are likely to be particularly informative.

Morphology and development of the haptors among the Monocotylidae (Monogenea)

Monocotylid monogeneans inhabit a wide diversity of sites on their chondrichthyan hosts including the skin, gills, nasal fossae, urogenital system and coelom. The large variation in the morphology of the haptor appears to reflect this diversity in attachment sites. We demonstrate that the complexity of the haptor can be related to the habitat of the parasite. Generally, those parasites which live in habitats subject to strong water currents such as the gills and dorsal skin surface have more complex haptors than those in environments exposed to weaker or no water currents including the nasal fossae, urogenital system and body cavity. However, there can be considerable variation in haptoral components, even among congeners, living on the ‘gills’ of their hosts. The microhabitat was determined for Monocotyle helicophallus and M. spiremae, both from the gills of the pink whipray, Himantura fai, and M. corali from the gills of the cowtail ray, Pastinachus sephen. We demonstrate that differences in the morphology of the hamuli and the number and morphology of septal sclerites and marginal papillae among these species of Monocotyle can be related directly to their microhabitat. It also appears that different haptoral structures are important for attachment to the host at different stages in the development of the parasite, based on studies on the development and distribution of Neoheterocotyle rhinobatidis from the gills of the common shovelnose ray Rhinobatos typus.

A revision of Neoheterocotyle (Monogenea: Monocotylidae) with descriptions of the larvae of N. rhinobatis and N. rhynchobatis from Heron Island, Great Barrier Reef, Australia

Rhinobatos typus and Rhynchobatus djiddensis were collected from Heron Island, Australia and examined for monocotylid parasites. Specimens of Neoheterocotyle rhinobatidis (Young, 1967) Chisholm, 1994 and N. rhynchobatis (Tripathi, 1959) Chisholm, 1994 were collected from the gills of Rhinobatos typus. This represents both a new host and new locality record for N. rhynchobatis. Neoheterocotyle bychowskyi (Timofeeva, 1981) Chisholm, 1994, N. nagibinae (Timofeeva, 1981) Chisholm, 1994 and N. rhinobatis (Pillai & Pillai, 1976) n. comb. were identified from the gills of Rhynchobatus djiddensis from Australia and are all new locality records. We consider N. djiddensis (Pillai & Pillai, 1976) n. comb. a species inquirenda and synonymise N. trilobata Timofeeva, 1981 with N. rhinobatis. Therefore, there are 7 valid species in the genus, including N. bychowskyi, N. forficata, N. inpristi, N. nagibinae, N. rhinobatidis, N. rhinobatis and N. rhynchobatis. The larvae of N. rhinobatis and N. rhynchobatis are described and the anterior glands of the larvae are related to those of the adults. The development of the male copulatory organ of N. rhinobatidis is described. Host-specificity and geographic range of the genus are also discussed and a key to species is provided.

A revision of Heterocotyle (Monogenea:Monocotylidae) with a description of Heterocotyle capricornensis n. sp. from Himantura fai (Dasyatididae) from Heron Island, Great Barrier Reef, Australia.

Heterocotyle capricornensis n. sp. is described from the gills of Himantura fai collected from Heron Island, Great Barrier Reef, Australia. It is distinguished from other species in the genus by the morphology of the sclerotised male copulatory organ which is curved and tapered distally, the ovary which loops once before entering the oviduct, and the testis which has 3 posteriorly-directed lobes. The oncomiracidium of this species is also described. The homology between glands found in the oncomiracidium and the adult is discussed. Additional data based on the examination of type material and, in some cases, new material of previously described species are included. The genus is revised and a key to species is provided. Characters which unite the members of the genus could not be confirmed for Heterocotyle elliptica Pillai & Pillai, 1976 and H. robusta (Johnston & Tiegs, 1992) Price, 1938 and therefore we consider them species inquirendae. New host and locality records are presented for H. chinensis Timofeeva, 1983 and a new host record is presented for H. granulatae Young, 1967. Host-specificity and phylogenetic relationships in Heterocotyle are discussed.

A revision of Dendromonocotyle Hargis, 1955 (Monogenea: Monocotylidae) with a description of a new species from Pastinachus sephen (Forsskal) (Myliobatiformes: Dasyatididae) from the Great Barrier Reef, Australia

The genus Dendromonocotyle contains seven previously described species: D. octodiscus Hargis, 1955; D. taeniurae Euzet and Maillard, 1967; D. kuhlii Young, 1967; D. cortesi Bravo-Hollis, 1969; D. akajeii Ho and Perkins, 1980; D. californica Olson and Jeffries, 1983; and D. centrourae Cheung and Whitaker, 1993. An eighth species, D. ardea sp. nov., is described from the dorsal body surface of the ray Pastinachus sephen (Forsskal) from Heron Island, Queensland, Australia. Dendromonocotyle ardea is distinguished from other species in the genus by the distinctive morphology of the terminal papillar sclerite, distal portion of the male copulatory organ and proximal portion of the vagina. An accessory chamber which may serve as a second seminal receptacle is also a differentiating character. Dendromonocotyle octodiscus, the type species of the genus, is redescribed and illustrated, and supplementary data and illustrations for features of the other species of the genus are provided. A key to the species of the g...

A revision of the Calicotylinae Monticelli, 1903(Monogenea: Monocotylidae)

A total of 153 elasmobranchs (46 species), either freshly collected from the Gulf of Mexico, USA and Tasmania, Australia or museum specimens collected from various localities worldwide, were examined for calicotyline (Monocotylidae) monogeneans. Thirty-five elasmobranchs, representing 17 species, were infected with Calicotyle spp. which we identified as the following previously described species: C. asterii (Szidat, 1970) Timofeeva, 1985, C. kroyeri Diesing, 1850, C. macrocotyle Cordero, 1944, C. similis (Szidat, 1972) Timofeeva, 1985, C. splendens (Szidat, 1970) Timofeeva, 1985, C. stossichi Braun, 1899 and C. urolophi Chisholm, Beverley-Burton & Last, 1991. The Calicotylinae, which comprises the genera Calicotyle and Dictyocotyle, is revised based on supplementary material as well as deposited type-material. We consider 14 of the 17 nominal Calicotyle spp. to be valid. C. rosinae Kusnetzova, 1970 is synonymised with C. macrocotyle, C. sjegi Kusnetzova, 1970 is considered a species inquirenda and C. inermis Woolcock, 1936 a species incertae sedis. Additional data and illustrations to show the morphological features of the hamuli and male copulatory organ, the form of the intestinal caeca, vaginae and ovary and the distribution of the vitellarium are provided for all valid species. The distribution of the 14 hooklets in the adult haptor of Dictyocotyle coeliaca Nybelin, 1941 is illustrated for the first time. We provide new host and locality records for C. asterii, C. kroyeri, C. macrocotyle and C. stossichi and new locality records for C. similis and C. splendens. A key to species of the Calicotylinae is also included. Host-specificity, geographical distribution and the need for information regarding the development of individuals from juvenile to adult are discussed.

Revision of Decacotylinae Chisholm, Wheeler & Beverley Burton, 1995 (Monogenea: Monocotylidae), including the synonymy of Papillicotyle Young, 1967 with Decacotyle Young, 1967 and a description of a new species from Australia

Close examination of type and new material of Decacotyle lymmae Young, 1967 revealed the presence of two unsclerotised structures on the dorsal surface of the haptor which were overlooked in the original description. We demonstrate that Papillicotyle Young, 1967, distinguished previously from Decacotyle Young, 1967 in part by the presence of unsclerotised accessory structures on the dorsal surface of the haptor, is synonymous with Decacotyle. D. tetrakordyle n. sp. is described from the gills of Pastinachus sephen (Forsskål) collected from Heron Island, Great Barrier Reef, Australia. D. tetrakordyle n. sp. is distinguished from the other four species in the genus by the presence of four accessory structures on the dorsal surface of the haptor and a complex male copulatory organ. Additional specimens of D. lymmae Young, 1967 from the gills of Taeniura lymma (Forsskål) and D. floridana (Pratt, 1910) n. comb and D. octona (Young, 1967) n. comb from the gills of Aetobatus narinari (Euphrasen) were also collected from the Queensland coast, Australia in the present study: D. youngi (Timofeeva, 1983) n. comb. is also transferred to Decacotyle from Papillicotyle. The Decacotylinae Chisholm, Wheeler & Beverley-Burton, 1995 is revised based on examination of type material, material of the new species and additional material of three previously described species. The oncomiracidium of D. floridana is described. A key to species is given and a description is provided of anterior glands containing needle-like secretion located lateral to the pharynx not described previously in D. lymmae. The discovery of D. floridana at Heron Island and D. octona in Moreton Bay represent new locality records for these species.

Descriptions of the larvae of six species of monocotylid monogeneans from Himantura fai (Dasyatididae) and Rhinobatos typus (Rhinobatidae) from Heron Island, Great Barrier Reef, Australia

The oncomiracidia of the following six species of monocotylids are described: Monocotyle helicophallus and M. spiremae from the gills and Merizocotyle australensis from the nasal fossae of Himantura fai; Neoheterocotyle rhinobatidis and Troglocephalus rhinobatidis from the gills and Merizocotyle icopae from the nasal fossae of Rhinobatos typus. With these descriptions, larvae from 17 described monocotylids representing 11 genera from five subfamilies are now known. The distribution, types of secretions, and possible functions of the anteromedian, lateral and posterior gland-cells are discussed. The distribution of flame-cells and other characters which may help distinguish between oncomiracidia of monocotylids are also tabulated and discussed.

Ultrastructure of the eyes of the larva of Neoheterocotyle rhinobatidis (Platyhelminthes, Monopisthocotylea), and phylogenetic implications

The oncomiracidium of Neoheterocotyle rhinobatidis (Monogenea, Monopisthocotylea, Monocotylidae) has two pairs of eyes, each eye with a lens and pigment cup. The anterior eyes have a single rhadomere; the posterior ones, two rhadomeres. Lenses are part of the pigment cup cells, as indicated by cytoplasmic connections between them and the pigment cups, and they are of mitochondrial origin because mitochondrial cristae are present in the periphery of the lenses. This is the first time that mitochondrial lenses have been shown to exist in a neodermatan. Such lenses may be a synapomorphy of a large taxon comprising the Neodermata and its turbellarian sister groups, or they may have evolved convergently in several not closely related groups as a result of strong selection pressure to find a suitable habitat or host.