Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-24T07:44:05.753Z Has data issue: false hasContentIssue false
  • English
  • Français

The survival of monogenean (platyhelminth) parasites on fish skin

Published online by Cambridge University Press:  16 October 2009

G. C. Kearn
G. C. Kearn
Affiliation:
School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Get access Rights & Permissions [Opens in a new window]

Summary

This review deals with the problems faced by those monogenean (platyhelminth) parasites that attach themselves to fish skin. The structure of the skin and the ways in which the posterior hook-bearing haptor achieves virtually permanent attachment to the skin are considered. Small marginal hooklets are specialized for attachment to superficial host epidermal cells, finding anchorage in the terminal web of keratinous tonofilaments, while large hooks (hamuli) may penetrate into and lodge in the collagenous dermis. The complementary roles of suction and sticky secretions in haptor attachment and the role of the pharynx in temporary attachment during feeding are also considered. During leech-like locomotion the haptor is briefly detached and, at this critical time, the anterior end is strongly fixed to the wet, current-swept and possibly slimy skin by a sticky secretion. This secretion is deployed on paired pads or discs, the latter sometimes backed up by suction. After attachment by the haptor is re-established, the special tegument covering the anterior adhesive areas may be instrumental in their instant release. The role of fish skin in the phenomenon of host specificity and in the generation of a defensive response against monogeneans is considered and site-specificity of parasites on the host's body is discussed. Possible selection pressures exerted by predatory ‘cleaner’ organisms are briefly evaluated.

Keywords

Monogeneansfish skinattachmenthost-specificityimmunitysite-specificitypredation
Type
Research Article
Information
Parasitology , Volume 119 , Supplement S1: Parasite Adaptation to Environmental Constraints , December 1999 , pp. S57 - S88
Copyright
Copyright © Cambridge University Press 1999

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bakke, T. A., Harris, P. D., Jansen, P. A. & Hansen, L. P. (1992). Host specificity and dispersal strategy in gyrodactylid monogeneans, with particular reference to Gyrodactylus salaris (Platyhelminthes, Monogenea). Diseases of Aquatic Organisms 13, 63–74.CrossRefGoogle Scholar
Bakke, T. A., Jansen, P. A. & Hansen, L. P. (1991). Experimental transmission of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) from the Atlantic salmon ( Salmo salar) to the European eel (Anguilla anguilla). Canadian Journal of Zoology 69, 733–737.CrossRefGoogle Scholar
Bakke, T. A., Jansen, P. A. & Harris, P. D. (1996). Differences in susceptibility of anadromous and resident stocks of Arctic charr to infections of Gyrodactylus salaris under experimental conditions. Journal of Fish Biology 49, 341–351.Google Scholar
Bereiter-Hahn, J., Richards, K. S., Eisner, L. & Voth, M. (1980). Composition and formation of flame cell caps: a substratum for the attachment of micro-organisms to sea horse epidermis. Proceedings of the Royal Society of Edinburgh 79B, 105–111.Google Scholar
Bondad-Reantaso, M. G., Ogawa, K., Yoshinaga, T. & Wakabayashi, H. (1995). Acquired protection against Neobenedenia girellae in Japanese flounder. Fish Pathology 30, 233–238.CrossRefGoogle Scholar
Buchmann, K. (1997). Population increase of Gyrodactylus derjavini on rainbow trout induced by testosterone treatment of the host. Diseases of Aquatic Organisms 30, 145–150.CrossRefGoogle Scholar
Buchmann, K. (1998). Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes: Monogenea). Diseases of Aquatic Organisms 32, 195–200.CrossRefGoogle ScholarPubMed
Buchmann, K. (1999). Immune mechanisms in fish skin against monogeneans – a model. Folia Parasitologica 46, 1–9.Google ScholarPubMed
Buchmann, K. & Bresciani, J. (1998). Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: association between mucous cell density in skin and site selection. Parasitology Research 84, 17–24.CrossRefGoogle ScholarPubMed
Buchmann, K. & Bresciani, J. (1999). Rainbow trout leucocyte activity: influence on the ectoparasitic monogenean Gyrodactylus derjavini. Diseases of Aquatic Organisms 35, 13–22.CrossRefGoogle ScholarPubMed
Buchmann, K. & Uldal, A. (1997). Gyrodactylus derjavini infections in four salmonids: comparative host susceptibility and site selection of parasites. Diseases of Aquatic Organisms 28, 201–209.CrossRefGoogle Scholar
Bullock, A. M., Marks, R. & Roberts, R. J. (1978 a). The cell kinetics of teleost fish epidermis: mitotic activity of the normal epidermis at varying temperatures in plaice (Pleuronectes platessa). Journal of Zoology 184, 423–428.CrossRefGoogle Scholar
Bullock, A. M., Marks, R. & Roberts, R. J. (1978 b). The cell kinetics of teleost fish epidermis: epidermal mitotic activity in relation to wound healing at varying temperatures in plaice (Pleuronectes platessa). Journal of Zoology 185, 197–204.CrossRefGoogle Scholar
Bychowsky, B. E. (1957). Monogenetic Trematodes – Their Systematics and Phylogeny. English translation by Hargis, W. J. (1961). Washington, American Institute of Biological Sciences.Google Scholar
Carvalho-Varela, M. & Cunha-Ferreira, V. (1987). Helminth parasites of the common sole, Solea solea, and the Senegalese sole, Solea senegalensis, on the Portuguese continental coast. Aquaculture, 67, 135–138.CrossRefGoogle Scholar
Chisholm, L. A. & Whittington, I. D. (1995). A revision of Dendromonocotyle Hargis, 1955 (Monogenea: Monocotylidae) with a description of a new species from Pastinachus sephen Forsskål (Myliobatiformes: Dasyatididae) from the Great Barrier Reef, Australia. Journal of Natural History 29, 1093–1119.CrossRefGoogle Scholar
Cone, D. & Burt, M. D. B (1981). The invasion route of the gill parasite Urocleidus adspectus Mueller, 1936 (Monogenea: Ancyrocephalinae). Canadian Journal of Zoology 59, 2166–2171.CrossRefGoogle Scholar
Cone, D. K. & Odense, p. H. (1984). Pathology of five species of Gyrodactylus Nordmann, 1832 (Monogenea). Canadian Journal of Zoology 62, 1084–1088.CrossRefGoogle Scholar
Cone, D. K. & Wiles, M. (1989). Ultrastructural study of attachment of Gyrodactylus colemanensis (Monogenea) to fins of fry of Salmo gairdneri. Proceedings of the Helminthological Society of Washington 56, 29–32.Google Scholar
Cribb, B. W., Whittington, I. D. & Chisholm, L. A. (1997). Observations on ultrastructure of the anterior adhesive areas and other anterior glands in the monogenean, Monocotyle spiremae (Monocotylidae), from the gills of Himantura fai (Dasyatididae). International Journal for Parasitology 27, 907–917.CrossRefGoogle ScholarPubMed
Cusack, R. & Cone, D. K. (1986). Gyrodactylus salmonis (Yin and Sproston, 1948) parasitizing fry of Salvelinus fontinalis (Mitchill). Journal of Wildlife Diseases 22, 209–213.CrossRefGoogle Scholar
Dollfus, R. P. & Euzet, L. (1964). Complément à la description de Pseudobenedenia nototheniae T. H. Johnston, 1931 (Trematoda Monogenea) parasite d'un téléostéen du genre Notothenia Richardson des Kerguelen (Mission Jean-Claude Hureau, 1963–1964). Bulletin du Muséum National d'Histoire Naturelle (2nd Series) 36, 849–857.Google Scholar
El-Naggar, M. M. (1992). Scanning electron microscope studies on the head lobes and haptor of the monogenean Gyrodactylus groschafti Ergens, 1973. Journal of the Egyptian German Society of Zoology 8 (B), Anatomy & Embryology, 435–445.Google Scholar
El-Naggar, M. M. & Kearn, G. c. (1983). Glands associated with the anterior adhesive areas and body margins in the skin-parasitic monogenean Entobdella soleae. International Journal for Parasitology 13, 67–81.CrossRefGoogle Scholar
El-Naggar, M. M. & Serag, H. M. (1987). Redescription of Macrogyrodactylus clarii Gusev 1961, a monogenean gill parasite of Clarias lazera in Egypt. Arab Gulf Journal of Scientific Research. Agricultural and Biological Sciences 5, 257–271.Google Scholar
Euzet, L. & Maillard, c. (1967). Parasites de poissons de mer ouest-africains, récoltés par J. Cadenat. VI. Monogènes de sélaciens. Bulletin de I'institut Fundamental d'Afrique Noire 29, 1435–1493.Google Scholar
Fletcher, T. C. (1978). Defence mechanisms of fish. In Biochemical and Biophysical Perspectives in Marine Biology, Vol. 4 (ed. Malins, D. C. & Sargent, J. R.), pp. 189–222. London, Academic Press.Google Scholar
Fletcher, T. C. & Grant, P. T. (1969). Immunoglobulins in the serum and mucus of the plaice (Pleuronectes platessa). Biochemical Journal 115, 65p.CrossRefGoogle ScholarPubMed
Fletcher, T. C., Jones, R. & Reid, L. (1976). Identification of glycoproteins in goblet cells of epidermis and gill of plaice ( Pleuronectes platessa L.), flounder ( Platichthys flesus (L.)) and rainbow trout ( Salmo gairdneri Richardson). Histochemical Journal 8, 597–608.CrossRefGoogle ScholarPubMed
Fletcher, T. C. & White, A. (1973). Antibody production in the plaice ( Pleuronectes platessa L.) after oral and parenteral immunization with Vibrio anguillarum antigens. Aquaculture 1, 417–428.CrossRefGoogle Scholar
Fuchs, E. & Hanukoglu, I. (1986). Epidermal α-keratins: structural diversity and changes during tissue differentiation. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, G. M. & Richards, K. S.), pp. 644–665. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Fujino, T., Ichikawa, H., Fukuda, K. & Fried, B. (1998). The expulsion of Echinostoma trivolvis caused by goblet cell hyperplasia in severe combined immunodeficient (SCID) mice. Parasite 5, 219–222.CrossRefGoogle ScholarPubMed
Halton, D. W. (1978). Trans-tegumental absorption of L-alanine and L-leucine by a monogenean, Diclidophora merlangi. Parasitology 76, 29–37.CrossRefGoogle ScholarPubMed
Harris, P. D. (1982). Variations in the mechanism of attachment in the Gyrodactyloidea (Monogenea). Parasitology 85, lviii.Google Scholar
Harris, P. D. (1986). Species of Gyrodactylus von Nordmann, 1832 (Monogenea Gyrodactylidae) from poeciliid fishes, with a description of G. turnbulli sp. nov. from the guppy, Poecilia reticulata Peters. Journal of Natural History 20, 183–191.CrossRefGoogle Scholar
Harris, P. D. (1988). Changes in the site specificity of Gyrodactylus turnbulli Harris, 1986 (Monogenea) during infections of individual guppies ( Poecilia reticulata Peters, 1859). Canadian Journal of Zoology 66, 2854–2857.CrossRefGoogle Scholar
Harris, P. D., Soleng, A. & Bakke, T. A. (1998). Killing of Gyrodactylus salaris (Platyhelminthes, Monogenea) mediated by host complement. Parasitology 117, 137–143.CrossRefGoogle ScholarPubMed
Harris, P. D., Soleng, A. & Bakke, T. A. (2000). Increased susceptibility of salmonids to the monogenean Gyrodactylus salaris following administration of hydrocortisone acetate. Parasitology 120, 57–64.CrossRefGoogle Scholar
Hidalgo Escalante, E. (1958). Hallazgo de una nueva especie de Capsala, Capsala pricei n. sp. (Trematoda, Monogenea) en un pez marino del puerto de Mazatlan Sinaloa, Mexico. Anales del Institute de Biologia, México 29, 209–217.Google Scholar
Hobson, E. S. (1974). Feeding relationships of teleostean fishes on coral reefs in Kona, Hawaii. Fishery Bulletin, U.S. Fish and Wildlife Service 72, 915–1031.Google Scholar
Horton, M. A. & Whittington, I. D. (1994). A new species of Metabenedeniella (Monogenea: Capsalidae) from the dorsal fin of Diagramma pictum (Perciformes: Haemulidae) from the Great Barrier Reef, Australia with a revision of the genus. Journal of Parasitology 80, 998–1007.CrossRefGoogle ScholarPubMed
Iger, Y., Jenner, H. A. & Wendelaar Bonga, S. E. (1994). Cellular responses in the skin of rainbow trout (Oncorhynchus mykiss) exposed to Rhine water. Journal of Fish Biology 45, 111, 9–1132.Google Scholar
Ishikawa, N., Horh, Y. & Nawa, Y. (1993). Immune-mediated alteration of the terminal sugars of goblet cell mucins in the small intestine of Nippostrongylus brasiliensis-infected rats. Immunology 78, 303–307.Google ScholarPubMed
Jahn, T. L. & Kuhn, L. R. (1932). The life history of Epibdella melleni MacCallum 1927, a monogenetic trematode parasitic on marine fishes. Biological Bulletin 62, 89–111.CrossRefGoogle Scholar
Jara, C., An, L. & Cone, D. (1991). Accessorius peruensis gen. et sp. n. (Monogenea: Gyrodactylidea) from Lebiasina bimaculata (Characidae) in Peru. Journal of the Helminthological Society of Washington 58, 164–166.Google Scholar
Kayton, R. J. (1983). Histochemical and X-ray elemental analysis of the sclerites of Gyrodactylus spp. (Platyhelminthes: Monogenoidea) from the Utah chub, Gila atraria (Girard). Journal of Parasitology 69, 862–865.CrossRefGoogle Scholar
Kearn, G. C. (1963 a). The oncomiracidium of Capsala martinieri, a monogenean parasite of the sun fish ( Mola mola). Parasitology 53, 449–453.CrossRefGoogle Scholar
Kearn, G. C. (1963 b). The egg, oncomiracidium and larval development of Entobdella soleae, a monogenean skin parasite of the common sole. Parasitology 53, 435–447.CrossRefGoogle Scholar
Kearn, G. C. (1963 c). Feeding in some monogenean skin parasites: Entobdella soleae on Solea solea and Acanthocotyle sp. on Raia clavata. Journal of the Marine Biological Association of the United Kingdom 43, 749–766.CrossRefGoogle Scholar
Kearn, G. C. (1964). The attachment of the monogenean Entobdella soleae to the skin of the common sole. Parasitology 54, 327–335.CrossRefGoogle Scholar
Kearn, G. C. (1965). The biology of Leptocotyle minor, a skin parasite of the dogfish, Scyliorhinus canicula. Parasitology 55, 473–480.CrossRefGoogle Scholar
Kearn, G. C. (1967 a). The life-cycles and larval development of some acanthocotylids (Monogenea) from Plymouth rays. Parasitology 57, 157–167.CrossRefGoogle Scholar
Kearn, G. C. (1967 b). Experiments on host-finding and host-specificity in the monogenean skin parasite Entobdella soleae. Parasitology 57, 585–605.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1968). The development of the adhesive organs of some diplectanid, tetraonchid and dactylogyrid gill parasites (Monogenea). Parasitology 58, 149–163.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1974). A comparative study of the glandular and excretory systems of the oncomiracidia of the monogenean skin parasites Entobdella Hippoglossi, E. diadema and E. soleae. Parasitology 69, 257–269.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1978). Entobdella australis, sp. nov., a skin-parasitic monogenean from the Queensland stingrays Taeniura lymma and Amphotistius kuhlii. Australian Journal of Zoology 26, 207–214.CrossRefGoogle Scholar
Kearn, G. C. (1988 a). Orientation and locomotion in the monogenean parasite Entobdella soleae on the skin of its host (Solea soled). International Journal for Parasitology 18, 753–759.CrossRefGoogle Scholar
Kearn, G. C. (1988 b). The monogenean skin parasite Entobdella soleae: movement of adults and juveniles from host to host (Solea solea). International Journal for Parasitology 18, 313–319.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1990). The rate of development and longevity of the monogenean skin parasite Entobdella soleae. Journal of Helminthology 64, 340–342.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1993). A new species of the genus Enoplocotyle (Platyhelminthes: Monogenea) parasitic on the skin of the moray eel Gymnothorax kidako in Japan, with observations on hatching and the oncomiracidium. Journal of Zoology 229, 533–544.CrossRefGoogle Scholar
Kearn, G. C. (1994). Evolutionary expansion of the Monogenea. International Journal for Parasitology 24, 1227–1271.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1998). Parasitism and the Platyhelminths. London, Chapman & Hall.Google Scholar
Kearn, G. C. & Evans-Gowing, R. (1998). Attachment and detachment of the anterior adhesive pads of the monogenean (platyhelminth) parasite Entobdella soleae from the skin of the common sole (Solea solea). International Journal for Parasitology 28, 1583–1593.CrossRefGoogle ScholarPubMed
Kearn, G. C. & Gowing, R. (1989). Glands and sensilla associated with the haptor of the gill-parasitic monogenean Tetraonchus monenteron. International Journal for Parasitology 19, 673–679.CrossRefGoogle Scholar
Kearn, G. C. & Gowing, R. (1990). Vestigial marginal booklets in the oncomiracidium of the microbothriid monogenean Leptocotyle minor. Parasitology Research 76, 406–408.CrossRefGoogle Scholar
Kearn, G. C., Ogawa, K. & Maeno, Y. (1992). Egg production, the oncomiracidium and larval development of Benedenia seriolae, a skin parasite of the yellowtail, Seriola quinqueradiata, in Japan. Publications of the Seto Marine Biological Laboratory 35, 351–362.CrossRefGoogle Scholar
Kearn, G. C., Whittington, I. D. & Evans-GOWING, R. (1995). Use of cement for attachment in Neocalceostomoides brisbanensis, a calceostomatine monogenean from the gill chamber of the blue catfish, Arius graeffei. International Journal for Parasitology 25, 299–306.CrossRefGoogle Scholar
Krieg, T. & Timpl, R. (1986). Protein components of the epidermal basement membrane. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S.), pp. 788–799. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Kritsky, D. C. (1978). The cephalic glands and associated structures in Gyrodactylus eucaliae Ikezaki and Hoffman, 1957 (Monogenea: Gyrodactylidae). Proceedings of the Helminthological Society of Washington 45, 37–49.Google Scholar
Kritsky, D. C. & Fennessy, C. J. (1999). Calicobenedenia polyprioni n. gen., n. sp. (Monogenoidea: Capsalidae) from the external surfaces of wreckfish, Polyprion americanus (Teleostei: Polyprionidae), in the north Atlantic. Journal of Parasitology 85, 192–195.CrossRefGoogle Scholar
Kritsky, D. C. & Fritts, T. H. (1970). Monogenetic trematodes from Costa Rica with the proposal of Anacanthocotyle gen. n. (Gyrodactylidae: Isancistrinae). Proceedings of the Helminthological Society of Washington 37, 63–68.Google Scholar
Lamothe-Argumedo, R. (1997). Nuevo arreglo taxonómico de la subfamilia Capsalinae (Monogenea: Capsalinae), clave para los géneros y dos combinaciones nuevas. Anales del Institute de Biologia, Mexico 68, 207–223.Google Scholar
Lester, R. J. G (1972). Attachment of Gyrodactylus to Gasterosteus and host response. Journal of Parasitology 58, 717–722.CrossRefGoogle ScholarPubMed
Littlewood, D. T. J, Rohde, K. & Clough, K. A. (1998). The phylogenetic position of Udonella (Platyhelminthes). International Journal for Parasitology 28, 1241–1250.CrossRefGoogle ScholarPubMed
Llewellyn, J. (1957). Host-specificity in monogenetic trematodes. In First Symposium on Host-specificity Among Parasites of Vertebrates, pp. 199–212. Neuchâtel, Paul Attinger.Google Scholar
Llewellyn, J. (1982). Host-specificity and corresponding evolution in monogenean flatworms and vertebrates. Mémoires du Muséum national d'Histoire naturelle, Série A, Zoologie 123, 289–301.Google Scholar
Llewellyn, J. (1984). The biology of Isancistrum subulatae n.sp., a monogenean parasitic on the squid, Alloteuthis subulata, at Plymouth. Journal of the Marine Biological Association of the United Kingdom 64, 285–302.CrossRefGoogle Scholar
Llewellyn, J. & Euzet, L. (1964). Spermatophores in the monogenean Entobdella diadema Monticelli from the skin of sting-rays, with a note on the taxonomy of the parasite. Parasitology 54, 337–344.CrossRefGoogle Scholar
Lobb, C. J. & Clem, L. W. (1981). The metabolic relationships of the immunoglobulins in fish serum, cutaneous mucus, and bile. Journal of Immunology 127, 1525–1529.CrossRefGoogle ScholarPubMed
Lyons, K. M. (1966). The chemical nature and evolutionary significance of monogenean attachment sclerites. Parasitology 56, 63–100.CrossRefGoogle ScholarPubMed
Lyons, K. M. (1969). Compound sensilla in monogenean skin parasites. Parasitology 59, 625–636.CrossRefGoogle Scholar
Lyons, K. M. (1973). Scanning and transmission electron microscope studies on the sensory sucker papillae of the fish parasite Entobdella soleae (Monogenea). Zeitschrift für Zellforschung 137, 471–480.CrossRefGoogle ScholarPubMed
Malmberg, G. & Fernholm, B. (1989). Myxinidocotyle gen. n. and Lophocotyle Braun (Platyhelminthes, Monogenea, Acanthocotylidae) with descriptions of three new species from hagfishes (Chordata, Myxinidae). Zoologica Scripta 18, 187–204.CrossRefGoogle Scholar
Malmberg, G. & Fernholm, B. (1991). Locomotion and attachment to the host of Myxinidocotyle and Acanthocotyle (Monogenea, Acanthocotylidae). Parasitology Research 177, 415–420.CrossRefGoogle Scholar
Matoltsy, A. G. & Bereiter-Hahn, J. (1986). Introduction. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S.), pp. 1–7. Berlin, Springer-Verlag.Google Scholar
Moore, M. M., Kaattari, S. L. & Olson, R. E. (1994). Biologically active factors against the monogenetic trematode Gyrodactylus stellatus in the serum and mucus of infected juvenile English soles. Journal of Aquatic Animal Health 6, 93–100.2.3.CO;2>CrossRefGoogle Scholar
Nigrelli, R. F. (1937). Further studies on the susceptibility and acquired immunity of marine fishes to Epibdella melleni, a monogenetic trematode. Zoologica 22, 185–192.Google Scholar
Nigrelli, R. F. & Breder, C. M. (1934). The susceptibility and immunity of certain marine fishes to Epibdella melleni, a monogenetic trematode. Journal of Parasitology 20, 259–269.CrossRefGoogle Scholar
Ogawa, K., Bondad-Reantaso, M. G., Fukudome, M. & Wakabayashi, H. (1995). Neobenedenia girellae (Hargis, 1955) Yamaguti, 1963 (Monogenea: Capsalidae) from cultured marine fishes of Japan. Journal of Parasitology 81, 223–227.CrossRefGoogle ScholarPubMed
Ogawa, K. & Egusa, s. (1981). The systematic position of the genus Anoplodiscus (Monogenea: Anoplodiscidae). Systematic Parasitology 2, 253–260.CrossRefGoogle Scholar
Olson, A. C. Jr & Jeffries, M. (1983). Dendromonocotyle californica sp. n. (Monogenea: Monocotylidae) from the bat ray, Myliobatis californica, with a key to species. Journal of Parasitology 69, 602–605.CrossRefGoogle Scholar
Pickering, A. D. & Richards, R. H. (1980). Factors influencing the structure, function and biota of the salmonid epidermis. Proceedings of the Royal Society of Edinburgh 79B, 93–104.Google Scholar
Rees, J. & Kearn, G. C. (1984). The anterior adhesive apparatus and an associated compound sense organ in the skin-parasitic monogenean Acanthocotyle lobianchi. Zeitschrift für Parasitenkunde 70, 609–625.CrossRefGoogle Scholar
Richards, G. R. & Chubb, J. C. (1996). Host response to initial and challenge infections, following treatment, of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on the guppy (Poecilia reticulata). Parasitology Research 82, 242–247.CrossRefGoogle Scholar
Richards, G. R. & Chubb, J. C. (1998). Longer-term population dynamics of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on adult guppies ( Poecilia reticulata) in 50–1 experimental arenas. Parasitology Research 84, 753–756.CrossRefGoogle Scholar
Roberts, R. J. & Bullock, A. M. (1980). The skin surface ecosystem of teleost fishes. Proceedings of the Royal Society of Edinburgh 79B, 87–91.Google Scholar
Rogers, W. A. (1967). Polyclithrum mugilini gen. et sp. n. (Gyrodactylidae: Polyclithrinae subfam.n.) from Mugil cephalus L. Journal of Parasitology 53, 274–276.CrossRefGoogle Scholar
Rogers, W. A. (1968). Swingleus polyclithroides gen. et sp. n. (Monogenea: Gyrodactylidae) from Fundulus grandis Baird and Girard. Tulane Studies in Zoology and Botany 16, 22–25.Google Scholar
Rohde, K. (1994). The minor groups of parasitic Platyhelminthes. Advances in Parasitology 33, 145–234.CrossRefGoogle ScholarPubMed
Rombout, J. H. W. M., Taverne, N., van de Kamp, M. & Taverne-Thiele, A. J. (1993). Differences in mucus and serum immunoglobulin of carp ( Cyprinus carpio L). Developmental and Comparative Immunology 17, 309–317.CrossRefGoogle ScholarPubMed
Roubal, F. R., Quartararo, N. & West, A. (1992). Infection of captive Pagrus auratus (Bloch & Schneider) by the monogenean, Anoplodiscus cirrusspiralis Roubal, Armitage & Rohde (Anoplodiscidae) in Australia. Journal of Fish Diseases 15, 409–415.CrossRefGoogle Scholar
Roubal, F. R. & Whittington, I. D. (1990). Observations on the attachment by the monogenean, Anoplodiscus australis, to the caudal fin of Acanthopagrus australis. International Journal for Parasitology 20, 307–314.CrossRefGoogle Scholar
Sakai, D. K. (1992). Repertoire of complement in immunological defense mechanisms of fish. Annual Review of Fish Diseases 1992, 223–247.CrossRefGoogle Scholar
Schliwa, M. (1975). Cytoarchitecture of surface layer cells of the teleost epidermis. Journal of Ultrastructure Research 52, 377–386.CrossRefGoogle ScholarPubMed
Scott, M. E. (1985). Dynamics of challenge infections of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata (Peters). Journal of Fish Diseases 8, 495–503.CrossRefGoogle Scholar
Scott, M. E. & Anderson, R. M. (1984). The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology 89, 159–194.CrossRefGoogle ScholarPubMed
Sengel, P. (1986). Epidermal-dermal interactions. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S.), pp. 374–408. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Shinn, A. P., Gibson, D. I. & Sommerville, C. (1995). A study of the composition of the sclerites of Gyrodactylus Nordmann, 1832 (Monogenea) using X-ray elemental analysis. International Journal for Parasitology 25, 797–805.CrossRefGoogle ScholarPubMed
Skerrow, D. (1986). Epidermal α-keratin: structure and chemical composition. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S.), pp. 621–643. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Spearman, R. I. C. (1973). The Integument: a Textbook of Skin Biology. London, Cambridge University Press.Google Scholar
Sproston, N. G. (1946). A synopsis of the monogenetic trematodes. Transactions of the Zoological Society of London 25, 185–600.CrossRefGoogle Scholar
Sterud, E., Harris, P. D. & Bakke, T. A. (1998). The influence of Gyrodactylus salaris Malmberg, 1957 (Monogenea) on the epidermis of Atlantic salmon, Salmo salar L., and brook trout, Salvelinus fontinalis (Mitchill): experimental studies. Journal of Fish Diseases 21, 257–263.CrossRefGoogle ScholarPubMed
Louis-Cormier, E. A. StOsterland, C. K. & Anderson, p. D. (1984). Evidence for a cutaneous secretory immune system in rainbow trout (Salmo gairdneri). Developmental and Comparative Immunology 8, 71–80.CrossRefGoogle Scholar
Uitto, J. (1986). Interstitial collagens. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S.), pp. 800–809. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Wells, P. R. & Cone, D. K. (1990). Experimental studies on the effect of Gyrodactylus colemanensis and G. salmonis (Monogenea) on density of mucous cells in the epidermis of fry of Oncorhynchus mykiss. Journal of Fish Biology 37, 599–603.CrossRefGoogle Scholar
West, A. J. & Roubal, F. R. (1998). Experiments on the longevity, fecundity and migration of Anoplodiscus cirrusspiralis (Monogenea) on the marine fish Pagrus auratus (Bloch & Schneider) (Sparidae). Journal of Fish Diseases 21, 299–303.CrossRefGoogle ScholarPubMed
Whitear, M. (1970). The skin surface of bony fishes. Journal of Zoology 160, 437–454.CrossRefGoogle Scholar
Whitear, M. (1986 a). Epidermis. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S.), pp. 8–38. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Whitear, M. (1986 b). Dermis. In Biology of the Integument. 2. Vertebrates (ed. Bereiter-Hahn, J., Matoltsy, A. G. & Richards, K. S.), pp. 39–64. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Whitear, M., Mittal, A. K. & Lane, E. B. (1980). Endothelial layers in fish skin. Journal of Fish Biology 17, 43–65.CrossRefGoogle Scholar
Whitear, M. & Moate, R. (1998). Cellular diversity in the epidermis of Raja clavata (Chondrichthyes). Journal of Zoology 246, 275–285.CrossRefGoogle Scholar
Whittington, I. D. (1996). Benedeniine capsalid monogeneans from Australian fishes: pathogenic species, site-specificity and camouflage. Journal of Helminthology 70, 177–184.CrossRefGoogle ScholarPubMed
Whittington, I. D. & Barton, D. P. (1990). A new genus of monogenean parasites (Capsalidae: Benedeniinae) from stingrays (Rajiformes: Dasyatidae) with a description of a new species from the long-tailed stingray Himantura uarnak Forsskål from Queensland, Australia. Journal of Natural History 24, 327–340.CrossRefGoogle Scholar
Whittington, I. D. & Cribb, B. W. (1998). Glands associated with the anterior adhesive areas of the monogeneans, Entobdella sp. and Entobdella australis (Capsalidae) from the skin of Himantura fai and Taeniura lymma (Dasyatididae). International Journal for Parasitology 28, 653–665.CrossRefGoogle ScholarPubMed
Whittington, I. D. & Cribb, B. W. (1999). Morphology and ultrastructure of the anterior adhesive areas of the capsalid monogenean parasites Benedenia rohdei from the gills and B. lutjani from the pelvic fins of Lutjanus carponotatus (Pisces: Lutjanidae). Parasitology Research 85, 399–408.CrossRefGoogle Scholar
Whittington, I. D., Cribb, B. W., Hamwood, T. E. & Halliday, J. A. (2000). Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas? International Journal for Parasitology 30, 305–320.CrossRefGoogle ScholarPubMed
Whittington, I. D. & Horton, M. A. (1996). A revision of Neobenedenia Yamaguti, 1963 (Monogenea: Capsalidae) including a redescription of N. melleni (MacCallum, 1927) Yamaguti, 1963. Journal of Natural History 30, 1113–1156.CrossRefGoogle Scholar
Whittington, I. D. & Kearn, G. C. (1993). 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. Journal of Natural History 27, 1–14.CrossRefGoogle Scholar
Whittington, I. D. & Kearn, G. C. (1995). A new calceostomatine monogenean from the gills and buccal cavity of the catfish Arius graeffei from Moreton Bay, Queensland, Australia. Journal of Zoology 236, 211–222.CrossRefGoogle Scholar
Yano, T. (1996). The nonspecific immune system: humoral defense. In The Fish Immune System: Organism, Pathogen, and Environment (ed. Iwama, G. & Nakanishi, T.), pp. 105–157. San Diego, Academic Press.CrossRefGoogle Scholar