Graham C. Kearn

The Eggs of Monogeneans

Publisher Summary This chapter illustrates the role of the eggs in the biology of monogenean parasites. The life cycles of monogeneans are relatively simple compared with those of other parasitic platyhelminths (cestodes and digeneans). Most monogeneans inhabit the skin and gills of fishes, and these sites are accessible to free-swimming larvae (oncomiracidia) hatching from freely deposited aquatic eggs. This simple life cycle has sufficient evolutionary plasticity to enable monogeneans to adapt to fishes living in a range of marine and freshwater habitats and with strikingly different ways of life, such as bottom-living flat-fishes and fast-moving pelagic species. Greater evolutionary potential is revealed by the remarkable survival of monogeneans on those fish-like ancestors of the tetrapods that colonized the terrestrial environment, leading to monogenean life cycles of sometimes surprising complexity. The chapter focuses on hatching rhythms and hatching factors, which in many monogeneans are of fundamental importance in infection of new hosts, and the intriguing changes in reproductive biology that have accompanied the progressive attenuation of the ties between tetrapod hosts and the aquatic environment. Monogeneans deserve special attention, because they provide opportunities for direct observation of the egg assembly process and display a surprising variety of egg shapes and egg appendages, which have attracted little functional interpretation. Monogeneans show a remarkable diversity in the shape and size of their eggs and in their egg appendages. The possible significance of the shapes and sizes of monogenean eggs is discussed in the chapter.

Evolutionary expansion of the Monogenea.

The evolutionary expansion of the monogeneans has taken place in parallel with the diversification of the fish-like vertebrates. In this article the main trends in monogenean evolution are traced from a hypothetical skin-parasitic ancestor on early vertebrates. Special consideration is given to the following topics: early divergence between skin feeders and blood feeders; diversification and specialization of the haptor for attachment to skin; transfer from host to host, viviparity and the success of the gyrodactylids; predation on skin parasites and camouflage; colonization of the buccal and branchial cavities; diversification and specialization of the haptor for attachment to the gills; phoresy in gill parasites; the development of endoparasitism and the origin of the cestodes; the success of dactylogyroidean gill parasites; the uniqueness of the polyopisthocotyleans; ovoviviparity and the colonization of the tetrapods. Host specificity has been the guiding force of coevolution between monogeneans and their vertebrate hosts, but the establishment of monogeneans on unrelated hosts sharing the same environment (host-switching) may have been underestimated. Host-switching has provided significant opportunities for evolutionary change of direction and is probably responsible for the establishment of monogeneans on cephalopod molluscs, on the hippopotamus and possibly on chelonians. There are indications that host-switching may be more common in monogeneans that spread by direct transfer of adults/juveniles from host to host. A limitation on the further expansion of monogeneans is the need for water for the dispersal of the infective larva (oncomiracidium).

Glands associated with the anterior adhesive areas and body margins in the skin-parasitic monogenean Entobdella soleae

Abstract Using the light microscope and TEM, a detailed study has been made of the different kinds of gland cell opening on the body surfaces of the adult and the oncomiracidium of E. soleae . Particular attention has been paid to the gland cells supplying the anterior adhesive areas and to those gland cells opening along the margins of the head region and body of the parasite. The oncomiracidia as well as immature parasites have three adjacent adhesive sacs on each side of the head and the adhesive regions of adults and oncomiracidia are supplied with two kinds of secretion. The most abundant secretion takes the form of rod-shaped bodies which, in the oncomiracidium and in the adult, are transported through ducts with multiple apertures, each aperture usually permitting the passage of a single rod. The second secretion consists of roughly spherical vesicles which differ in appearance in oncomiracidia and adults. Most of these ducts appear to have single apertures but there is evidence in the adult that some of them branch and lead to more than one opening. The roles of these two kinds of secretion in attachment and detachment of the head region, in immature and in adult parasites, were studied experimentally. In immature and mature parasites ultrastructural studies reveal similarities between the secretory bodies produced by the anterior median head glands and those produced by gland cells opening on or near the body margins. Possible functions of the secretions of the marginal gland cells are discussed.

The biology of Leptocotyle minor , a skin parasite of the dogfish, Scyliorhinus canicula

Leptocotyle minor is a monogenean parasite specialized for living on the denticlecovered skin of the dogfish Scyliorhinus canicula . Each adult parasite attaches itself to the outer surface of a single denticle. Small postlarvae are found on the inner surfaces of the denticles. The denticles have hard enamel on both inner and outer exposed surfaces. Haptoral hooks, such as are present in other monogenean oncomiracidia, would be unable to penetrate this hard surface and are absent in postlarval and adult parasites which attach themselves by cement. The oncomiracidium possesses six haptoral spicules which may be homologues of the marginal hooks of other monogeneans, but these spicules disappear early in postoncomiracidial development. Adult parasites feed on the hosts epidermis which lies between the denticles. The position of small postlarvae on the inner surfaces of the denticles enables them to reach the epidermis for feeding purposes. Growth then permits young parasites to migrate away from the epidermis on to the outer surfaces of the denticles. Adult parasites move from one denticle to another in a leech-like manner, and copulation occurs between parasites which meet as a result of these movements. I am grateful to the Director and Staff of the Plymouth Laboratory for their hospitality and particularly to Mr J. E. Green for his interest and co-operation.

Observations on egg production in the monogenean Entobdella soleae

Abstract Egg production in the monogenean Entobdella soleae increases as adult parasites grow. Medium-sized adults (anterior hamulus length 550–600 μm; total body length approx. 5 mm) produced about 30 eggs per day at 12°C. Parasites with anterior hamuli exceeding 650 μm in length (total body length about 6 mm) may produce more than 60 eggs per day. In smaller adults, eggs tend to spend longer in the ootype after assembly of the shell and the ootype remains empty for longer periods of time. The time taken to assemble a single egg is relatively constant (4–6 min) in adults of all sizes and there is evidence of a small but significant increase in egg size as parasites increase in size. Some eggs were retained in the uterus for as long as 168 min but others spent less than 5 s in the uterus, indicating that the uterus is no more than a passageway for these eggs to the outside world. The egg cell (or zygote) precedes the vitelline cells as they progress along the ovo-vitelline duct to the ootype.

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.

Ultrastructural observations on the anterior adhesive apparatus in the monogeneans Dactylogyrus amphibothrium Wagener, 1857 and D. hemiamphibothrium Ergens, 1956.

The light microscope and the transmission electron microscope have revealed that the anterior adhesive apparatus ofDactylogyrus amphibothrium and that ofD. hemiamphibothrium are similar and composed of three kinds of gland cell, one producing rod-shaped bodies (secretion S1), one producing spherical bodies (S2), and the third producing electronlucent vesicles (S3). In the cytoplasm of Gl gland cells each rod-shaped body is enclosed by a single layer of microtubules but no microtubules are associated with S2 and S3 bodies. The possible functions of these microtubules are discussed. The ducts which extend anteriorly from all three kinds of gland cell coverge on and open into six adhesive sacs, situated ventrally on the distal extremities of the head lobes. Each adhesive sac is supplied with at least one gland duct from each type of gland cell and is lined by a special tegument bearing dense microvilli and a few cilia which may have a sensory function. It has been shown that during the attachment of the head region, these sacs are everted to expose the enclosed microvilli and duct openings and secretions S1 and S2 are extruded.

Ultrastructural and histochemical observations on the pigmented eyes of the oncomiracidium of Entobdella soleae, a monogenean skin parasite of the common sole, Solea solea

SummaryThe pigmented eyes of the oncomiracidium of the monogenean skin parasite Entobdella soleae are rhabdomeric in nature, the smaller anterior eyes each containing a single rhabdomere and the larger posterior eyes each containing two rhabdomeres. Each eye has a lens and a single cup-shaped pigment cell. There are differences in the arrangement of the microvilli in the rhabdomeres of the anterior and posterior eyes. Microvilli from each side of the anterior retinular cell are convergent. In each rhabdomere of the posterior eyes most of the microvilli lie parallel to each other but their direction is perpendicular to that of the microvilli of the adjacent posterior rhabdomere. The retinular cell leaves the eye between the pigment cell and the lens, and the retinular cell nucleus lies outside the eye. The darkbrown pigment in the pigment cell was identified as melanin. The lens contains carbohydrate and possibly protein but tests for fat were negative.

The oncomiracidia of the monocotylid monogeneans Dictyocotyle coeliaca and Calicotyle kroyeri

The eggs of D. coeliaca have been cultured successfully and the free-swimming larva has been studied for the first time. The eggs have an incubation period which for monogeneans is exceptionally long (4–5 months at 10 °C). Apart from maintenance at a low temperature no other special conditions such as high hydrostatic pressure or washing to remove host body fluid are necessary for development. It is not necessary for the eggs to come into contact with host body fluid before development can begin. The oncomiracidium of D. coeliaca has no eyes, a well-developed pair of anterior median gland cells and a pair of hamuli. The oncomiracidium of C. kroyeri is similar to that of D. coeliaca except for the presence of two pairs of conspicuous pigmented eyes, poorly developed anterior median gland cells, the presence of an extra pair of gland cells at the posterior end of the body and the absence of hamuli. A comparison of the larval features of D. coeliaca and C. kroyeri has confirmed that these parasites belong to quite distinct species.

Rhythmical Hatching and Oncomiracidial Behaviour in the Hexabothriid Monogenean Rajonchocotyle Emarginata from the Gills of Raja spp.

In a study of the life-cycle of the hexabothriid monogenean Rajonchocotyle emarginata by Wiskin (1970), attempts to obtain newly hatched larvae were unsuccessful, and it was decided to make a new attempt to culture eggs and hatch larvae, at the same time investigating the effects of those factors found in other monogeneans to influence hatching, such as host mucus (see Kearn, 1974), shadows (see Kearn, 1982) and mechanical disturbance (see Bovet, 1967). The success of these renewed attempts to hatch the eggs of R. emarginata provided an opportunity to study the behaviour of the free-swimming oncomiracidium and attempts were made to relate hatching phenomena and larval behaviour to the behaviour of the host.