Ian D. Whittington

A revision of Neobenedenia Yamaguti, 1963 (Monogenea : Capsalidae) including a redescription of N. melleni (MacCallum, 1927) Yamaguti, 1963

Neobenedenia Yamaguti, 1963, a genus of capsalid (benedeniine) monogeneans lacking a vagina, is redefined. The generic diagnosis is amended to include previously unused characters like the path of tendons in the haptor from extrinsic muscles in the body, the presence and form of a marginal valve, the shape of the anterior attachment organs, the arrangement of musculature at the posterior (proximal) end of the penis sac and the presence of a pair of sphincters in the female reproductive tract. On this basis, the generic composition is reduced from 10 to six species. Species considered valid are: N. melleni (MacCallum, 1927) Yamaguti, 1963; N. adenea (Meserve, 1938) Yamaguti, 1963; N. isabellae (Meserve, 1938) Yamaguti, 1963; N. longiprostata Bravo-Hollis, 1971; N. muelleri (Meserve, 1938) Yamaguti, 1963; N. pacifica Bravo-Hollis, 1971. Neobenedenia girellae (Hargis, 1955) Yamaguti, 1963 and N. paragueraensis Dyer, Williams and Bunkley-Williams, 1992 are considered synonyms of N. melleni. Species formerly a...

Diversity “down under”: monogeneans in the Antipodes (Australia) with a prediction of monogenean biodiversity worldwide

There are approximately 25,000 species of fishes known in the world. The Monogenea are believed to be among the most host-specific of parasites and if each species of fish is host to a different species of monogenean, there could be almost 25,000 monogenean species on Earth. Currently, I estimate that between 3000 and 4000 of these are described. Australia has a rich marine fish fauna with approximately 3500 species of teleosts. If the same formula of one monogenean species per host fish species is applied, Australia marine fishes could host potentially 3500 species of monogeneans. The first monogenean species described from Australia was Encotyllabe pagrosomi MacCallum, 1917 and approximately 300 more species have since been described from the continent. Even in a region of Australia such as Heron Island on the Great Barrier Reef that has been a focus of sustained research on these parasites, only about 85 species are described from 40 of the most common, easily-caught species of fish. Reasons are discussed for the relatively small numbers of monogenean species described so far from Australia. Endemicity is difficult to judge, but only one is certain: Concinnocotyla australensis (Polystomatidae) from Neoceratodus forsteri (Dipnoi). Despite reductions in research funding, the value of parasite taxonomy must not be underestimated, particularly in regions of the world that have a rich diversity of potential hosts.

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.

Closing the mitochondrial circle on paraphyly of the Monogenea (Platyhelminthes) infers evolution in the diet of parasitic flatworms

Relationships between the three classes of Neodermata (parasitic Platyhelminthes) are much debated and restrict our understanding of the evolution of parasitism and contingent adaptations. The historic view of a sister relationship between Cestoda and Monogenea (Cercomeromorphae; larvae bearing posterior hooks) has been dismissed and the weight of evidence against monogenean monophyly has mounted. We present the nucleotide sequence of the complete mitochondrial (mt) genome of Benedenia seriolae (Monogenea: Monopisthocotylea: Capsalidae), the first complete non-gyrodactylid monopisthocotylean mt genome to be reported. We also include nucleotide sequence data for some mt protein coding genes for a second capsalid, Neobenedenia sp. Analyses of the new mt genomes with all available platyhelminth mt genomes provide new phylogenetic hypotheses, which strongly influence perspectives on the evolution of diet in the Neodermata. Our analyses do not support monogenean monophyly but confirm that the Digenea and Cestoda are each monophyletic and sister groups. Epithelial feeding monopisthocotyleans on fish hosts are basal in the Neodermata and represent the first shift to parasitism from free-living ancestors. The next evolutionary step in parasitism was a dietary change from epithelium to blood. The common ancestor of Digenea+Cestoda was monogenean-like and most likely sanguinivorous. From this ancestral condition, adult digeneans and cestodes independently evolved dietary specialisations to suit their diverse microhabitats in their final vertebrate hosts. These improved perspectives on relationships fundamentally enhance our understanding of the evolution of parasitism in the Neodermata and in particular, the evolution of diet.

Benedeniine capsalid monogeneans from Australian fishes: pathogenic species, site-specificity and camouflage.

There are about 70 species of capsalid monogeneans in the Benedeniinae worldwide but only about half are described from the diverse fish fauna in the Pacific Ocean. Up to 1992, only five species of benedeniines were known from Australia. Two potentially destructive species of benedeniines, Benedenia seriolae from Seriola lalandi and B. sciaenae from Argyrosomus hololepidotus from temperate Australian waters, are new host and geographic records for these monogeneans. A survey of some fishes from the Great Barrier Reef has revealed at least 15 undescribed species of benedeniines in addition to three species which have been described recently (B. lutjani, B. rohdei and Metabenedeniella parva). The few previous records for benedeniines from Australian fishes are probably the result of three factors. First, there have been relatively few careful studies of the external surfaces of fishes from Australia for monogeneans. Second, some benedeniines display a previously unsuspected specificity for particular external microhabitats on their hosts such as specific fins or sites previously unrecognized as microhabitats for monogeneans on the head of some species of fishes such as lip folds and branchiostegal membranes. Third, some benedeniines on the flanks and fins of some fish are extremely difficult to see because they are transparent and/or possess pigment spots throughout the body. Sometimes, benedeniines from colourful species of reef fish bear bright colours in their bodies. It is highly likely that these features serve as camouflage to conceal the parasites from predators such as cleaner organisms.

Looks can deceive: Molecular phylogeny of a family of flatworm ectoparasites (Monogenea: Capsalidae) does not reflect current morphological classification

The morphological based taxonomy of highly derived parasite groups is likely to poorly reflect their evolutionary relationships. The taxonomy of the monogenean family Capsalidae, which comprises approximately 180 species of flatworm parasites that predominantly attach to external surfaces of chondrichthyan and teleost fishes, is based mainly on six morphological characters. The phylogenetic history of the family is largely unknown. We reconstructed the phylogenetic relationships of 47 species in 20 genera from eight of the nine subfamilies, from nucleotide sequences of three unlinked nuclear genes, 28S ribosomal RNA, Histone 3 and Elongation Factor 1 alpha. Our phylogeny was well corroborated, with 75% of branches receiving strong support from both Bayesian posterior probabilities and maximum likelihood bootstrap proportions and all nodes showed positive partitioned likelihood support for each of the three genes. We found that the family was monophyletic, with the Gyrodactylidae and Udonellidae forming the sister group. The Capsalinae was monophyletic, however, our data do not support monophyly for the Benedeniinae, Entobdellinae and Trochopodinae. Monophyly was supported for Capsala, Entobdella, Listrocephalos, Neobenedenia and Tristoma, but Benedenia and Neoentobdella were polyphyletic. Comparisons of the distribution of character states for the small number of morphological characters on the molecular phylogeny show a high frequency of apparent homoplasy. Consequently the current morphological classification shows little correspondence with the phylogenetic relationships within the family.

A view of early vertebrate evolution inferred from the phylogeny of polystome parasites (Monogenea: Polystomatidae)

The Polystomatidae is the only family within the Monogenea to parasitize sarcopterygians such as the Australian lungfish Neoceratodus poisteri and freshwater tetrapods (lissamphibians and chelonians). We present a phylogeny based on partial 18S rDNA sequences of 26 species of Polystomatidae and three taxon from the infrasubclass Oligonchoinea (= Polyopisthocotylea) obtained from the gills of teleost fishes. The basal position of the polystome from lungfish within the Polystomatidae suggests that the family arose during the evolutionary transition between actinopterygians and sarcopterygians, ca. 425 million years (Myr) ago. The monophyly of the polystomatid lineages from chelonian and lissamphibian hosts, in addition to estimates of the divergence times, indicate that polystomatids from turtles radiated ca. 191 Myr ago, following a switch from an aquatic amniote presumed to be extinct to turtles, which diversified in the Upper Triassic. Within polystomatids from lissamphibians, we observe a polytomy of four lineages, namely caudatan, neobatrachian, pelobatid and pipid polystomatid lineages, which occurred ca. 246 Myr ago according to molecular divergence–time estimates. This suggests that the first polystomatids of amphibians originated during the evolution and diversification of lissamphibian orders and suborders ca. 250 Myr ago. Finally, we report a vicariance event between two major groups of neobatrachian polystomes, which is probably linked to the separation of South America from Africa ca. 100 Myr ago.

A new species of skin-parasitic benedeniine monogenean with a preference for the pelvic fins of its host, Lutjanus carponotatus (Perciformes: Lutjanidae) from the Great Barrier Reef

Benedenia lutjani sp. nov. is described from the body surfaces and fins of the marine teleost, Lutjanus carponotatus (Richardson 1842) from Heron Island and Lizard Island, Queensland, Australia. The vaginal pore of the parasite opens on the dorsal surface anterior to the common genital aperture. There is a pair of lobes associated with the common genital aperture and a single lobe close to the vaginal opening. The diagnoses of the following taxa are amended: Benedeniinae and Benedenia. This is the first record of a species of Benedenia from the Lutjanidae. The oncomiracidium of B. lutjani is described. Evidence from freshly caught fishes and from a heavily infected aquarium-held host indicates that adult specimens of B. lutjani have a preference for the pelvic fins of L. carponotatus.

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.

Hatching rhythms in the capsalid monogeneans Benedenia lutjani from the skin and B. rohdei from the gills of Lutjanus carponotatus at Heron Island, Queensland, Australia

Spontaneous hatching of eggs of Benedenia lutjani and B. rohdei occurred after incubation for 4-6 days and 6-10 days, respectively, at a constant temperature in the range 22-28 degrees C when exposed to natural illumination or to alternating 12-h periods of light and darkness (LD12:12; light on, 06.00 h; light off, 18.00 h). Under these conditions, hatching of the eggs of both species was rhythmical, all larvae emerging only during periods of illumination. Hatching was not confined to particular times with the illuminated period. Evidence for an endogenous component to the rhythm was revealed by transfer of eggs from LD12:12 to continuous darkness (DD) near the end of the incubation period. Hatching, also occurred only during periods of illumination when eggs of each species were incubated under a DL12:12 regime (i.e. period of illumination 18.00 h to 06.0 h; period of darkness 06.00 h to 18.00 h). When the eggs of B. lutjani and B. rohdei were laid and incubated in DD or continuous illumination (LL), some degree of rhythmicity persisted, raising the possibility that the eggs inherit circadian rhythmicity from their parent. The hatching patterns of these 2 species of monogeneans are discussed in relation to host finding, host behaviour and limited observations on the behaviour of the oncomiracidia after hatching.