The Gyrocotylidea: an aberrant group of tapeworms

Authors

Background

The Gyrocoylidea is a small group of parasitic flatworms comprising ten known species in two genera,GyrocotyleandGyrocotyloides(although there has been much confusion about species identities, see e.g.,[1]). They are about 2-3 cm in length and infect the digestive tract of Holocephali, a group of marine chondrichthyen fishes (chimaeras, ratfishes), which are found in the deepsea and cold surface waters. Like the Amphilinidea, with whom they are sometimes grouped in the Cestodaria, they have 10 posterior hooks (easily visible only in the larvae) and lack proglottids characteristic of almost all eucestodes (genuine tapeworms). They belong to the Neodermata, which include all major groups of parasitic Platyhelminthes (flatworms) and, together with the Eucestoda and Amphilinidea, they form one monophylum (derived from one common ancestor), the Cestoda (tapeworms, Figure 1) [2]. They are without any economic importance, but have baffled biologists because of some unique morphological and biological features [3].


Figure 1. Phylogeny of the Neodermata (= major goups of parasitic flatworms) based on a cladistic analysis of DNA and morphological data. Note that the cestodes have one common ancestor, from which only they and no other group has evolved, i.e., they are monophyletic. Based on but strongly modified from Littlewood et al. 1999 [4]. See also [5].

Structure of the adult

Like all Neodermata, the surface layer of adult gyrocotylideans is a neodermis, i.e., a syncytial non-ciliated epidermis which replaces the ciliated epidermis of the larva. They lack an intestine, and the attachment organ in species of the genusGyrocotyleis a ruffled structure, the so-called rosette (Figures 2, 3 and 4). In the genusGyrocotyloides, the rosette is cup-like and located on a caudal stalk. A so-called funnel in the posterior part of the body opens dorsally through a pore, its function is unknown (but contributes possibly to attachment). The protonephridial system of the adult consists of flame bulbs and a network of capillaries and ducts. The paired excretory pores open not far from the anterior end. – Gyrocotylids are hermaphroditic. Follicular testes in the anterior part of the body are connected to sperm ducts which unite to form one large sperm duct whose terminal part is muscular forming an ejaculatory duct. It opens near the anterior end. The female reproductive system consists of an ovary composed of many small follicles, in the posterior part of the body. The oviduct, into which the egg cells are discharged, leads to the ootype surrounded by a shell or Mehlis’ gland, into which or near which the yolk duct and vagina open as well. Vitelline (yolk) follicles are scattered throughout most of the body. Eggs (fertilized egg cells and yolk surrounded by a shell) are formed in the ootype. Fertilized eggs pass into the uterus which opens near the anterior end, as does the vagina. – The main parts of the nervous system consist of anterior ganglia (aggregation of nerve cells) and larger posterior ones close to the rosette, connected by large connectives (longitudinal nerve cords). – Gyrocotylids, like all tapeworms, lack an intestine, food is absorbed through the tegument drawn out into numerous microvilli (Figure 5).


Figure 2. Gyrocotyle urna, rosette left. Original Willi Xylander. © Willi Xylander


Figure 3. AdultGyrocotyle fimbriata, dorsal view. Female reproductive system except vitellaria drawn red. Redrawn and strongly modified after Lynch (1945[6]) from Cheng (1986) [7] and other sources. © Klaus Rohde

Figure 4. Scanning electron-micrograph of the rosette ofGyrocotyle sp., probably G. rugosa, from the holocephalanCallorhinchus miliiin Tasmania. Original Klaus Rohde. © Klaus RohdeFigure


5. Scanning electron-micrograph of the tegument of Gyrocotyle sp., probablyG. rugosa,from the holocephalanCallorhinchus miliiin Tasmania. Note the numerous microvilli. Original Klaus Rohde. © Klaus Rohde

Structure of the larva

The so-called lycophora larva (lycophore) possesses 10 posteriorly located hooks and (at least in some species) a ciliated epidermis. There are two pairs of anterior gland cells, each pair with a different secretion. The protonephridial (excretory/osmoregulatory system) consists of a small number of flame bulbs connected to capillaries, which unite to form two large ducts with anterior excretory pores. Ciliary/lamellar photoreceptors are located at the anterior margin of the brain (Figure 6). Xylander has made detailed ultrastructural studies of the glandular system, protonephridia, nervous system and sensory receptors, and hooks of the larva of Gyrocotyle urna. He described seven receptor types (with a single cilium or non-ciliate) and a ciliate-lamellated presumptive photoreceptor, from the larva ofGyrocotyle urna [8].


Figure 6. Larva of Gyrocotyle urna. Redrawn and strongly modified from two figures by Xylander (1990 [9]) in Rohde (1994 [10]). © Klaus Rohde

Life cycle

The lycophora larva hatches from the egg. Attempts to work out the complete life cycle of any gyrocotylid have failed so far, although attempts were made to do this forGyrocotyle urna (Ruzskowski 1932 [11] and Simmons 1974 [3]). Host individuals are usually (but not always) infected by only one gyrocotylid species, but each holocephalan host species can harbour two species, usually attached to different sites along their spiral valve. One of each species pair belongs to the so-called ‘urna’, the other to the ‘confusa’ group. The former has many marginal body undulations and very elaborate folds of the rosette, whereas the latter has a smaller rosette with fewer folds, a more elongate body and less elaborate body undulations. Young hosts may harbour many, larger ones generally not more than two parasites. – Interestingly, so-called post-larvae, i.e. fully developed gyrocotylids, may be present in the parenchyma of gyrocotylids of the same species (e.g.,[12]). They seem to disintegrate after a while. Xylander (2005) [13] lists reasons why he believes that gyrocotylids have indirect life cycles, i.e. utilize an intermediate host, possibly a small crustacean (see also[14]).Ecological/economic importancePathogenic effects on hosts are usually not obvious and restricted to heavily infected individuals. In view of the small number of species occurring on a small host group (chimaeras), the group is unlikely to have any economic and probably negligible ecological importance.

References

Bristow, G. 1992. On the distribution, ecology and evolution of Gyrocotyle urna, G.confusa and G.nybelini (Cercomeromorpha:Gyrocotylidea) and their host Chimaera monstrosa (Holocephalida: Chimaeridae) in Norwegian waters, with a review of the species question. Sarsia 77, 119-124.Ehlers, U. 1985. Das phylogenetische System der Plathelminthes. Gustav Fischer Verlag, Stuttgart New York.Simmons, J.E. 1974. Gyrocotyle, a century-old enigma. In: W.B. Vernberg ed. Symbiosis in the Sea, University of South Carolina Press, Columbia SC, pp. 195-218.Littlewood D.T.J., Rohde, K., Bray, R.A. and Herniou, E.A. 1999. Phylogeny of the Platyhelminthes and the evolution of parasitism. Biological Journal of the Linnean Society , 68, 257-287.Xylander, W.E.R. 2001. Gyrocotylidea, Amphilinidea and the early evolution of Cestoda. In: D.J.T. Littlewood and R.A. Bray eds. Interrelationships of the Platyhelminthes, Taylor&Francis, London, pp. 103-111Lynch, J.E. 1945. Redescription of the species of Gyrocotyle from the ratfish, Hydrolagus colliei (Lay and Bennett), with notes on the morphology and taxonomy of the genus. Journal of Parasitology 31, 418-446.Cheng, T.C. 1986. General Parasitology, 2nd ed. Academic Press College Division, Harcourt Brace Jovanovich Publ., OrlandoXylander, W.E.R. 1987. Ultrastructure of the lycophora larva of Gyrocotyle urna (Cestoda, Gyrocotylidea). II. Receptors and nervous system. Zoologischer Anzeiger 219, 239-255.Xylander, W. 1990. Ultrastructure of the lycophora larva of Gyrocotyle urna (Cestoda, Gyrocotylidea). IV. The glandular system. Zoomorphology 109, 319-328.Rohde, K. 1994. The minor groups of parasitic Platyhelminthes. Advances in Parasitology, 33, 145-234.Ruszkowski, J.S. 1932. Etudes sur le cycle evolutiv et sur la structure des cestodes de mer.II. Sur les larves de Gyrocotyle urna (Gr. et Wagen.). Bull. Int. Acad. Pol. Sci. Lett. Cl. Sci. Math. Natur. B, 629-641.Halvorsen, O. and Williams, H.H. 1968. Studies of the helminth fauna of Norway. IX. Gyrocotyle (Platyhelminthes) in Chimaera monstrosa from Oslo Fjord, with emphasis on its mode of attachment and a regulation in the degree of infection. Nytt Magasin for Zoolopgy 15, 130-142.Xylander, W. 2005. Gyrocotylidea (unsegmented tapeworms). In: K. Rohde ed. Marine Parasitology. CSIRO Publishing Melbourne and CABI Wallingford Oxon., pp.89-92.Xylander, W.E.R.1989. Untersuchungen zur Biologie von Gyrocotyle urna (Cestoda) und Überlegungen zu ihrem Lebenszyklus. Verhandlungen der Deutschen Zoologischen Gesellschaft 82, 251.Rohde, K. 2007. Gyrocotylidea. In: McGraw-Hill Encyclopedia of Science and Technology, vol. 8, 313. McGraw-Hill, New York. ISBN: 0079136656Related knolsLinks to other parasitological knols by Klaus Rohde here.

See also: Rohde, K. 2007 [15].

Acknowledgement

I wish to thank Professor Willi Xylander, Senckenberg- Museum Görlitz, for the photo ofGyrocotyle urna(Figure 2).

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