Skip to main content
Log in

Sperm transfer in monogenean (platyhelminth) parasites

  • Invited Review
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

There are three major groups of parasitic platyhelminths (flatworms). The digeneans and cestodes are endoparasites, while the monogeneans are ectoparasites mostly on the gills or skin of fishes. Monogeneans are hermaphrodite and, with the exception of the gyrodactylids, mostly protandrous, the male reproductive system maturing before the female system. Their ectoparasitic life-style provides unique opportunities to observe the reproductive biology of living platyhelminths, opportunities restricted in digeneans and cestodes by their endoparasitic habits. Moreover, the male copulatory organs (MCOs) of monogeneans are of special interest because of their perplexing diversity, ranging from sclerotised penis tubes, many with accessory sclerites, to cirruses and genital atrium armature (hooks and spines). The relatively few accounts in the literature of mating in monogeneans are reproduced in this review, together with consideration of the following aspects of sperm transfer: structure and function of MCOs; self-insemination; spermatophores and pseudospermatophores; “hypodermic” and transtegumental insemination; tissue fusion; glands associated with MCOs and vaginae; finding a mating partner.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ainsworth C. 2005. The secret life of sperm. Nature, 436, 770–771. DOI: 10.1038/436770a

    Article  CAS  Google Scholar 

  • 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 (Platy-helminthes, Monogenea). Diseases of Aquatic Organisms, 13, 63–74. DOI: 10.3354/dao013063

    Article  Google Scholar 

  • Beverley-Burton M., Klassen G.J., Lester R.J.G. 1987. Generic diagnosis of Asthenocotyle Robinson, 1961 (Monogenea: Microbothriidae) and description of Asthenocotyle taranakiensis new species from Oxynotus bruniensis (Oxynotidae) taken in New Zealand waters. International Journal for Parasitology, 17, 965–969. DOI: 10.1016/0020-7519(87)90016-6

    Article  CAS  Google Scholar 

  • Beverley-Burton M., Whittington I.D. 1995. Clemacotyle australis (Monogenea: Monocotylidae) from the white-spotted eagle ray Aetobatus narinari (Rajiformes: Myliobatididae) on the Great Barrier Reef: redescription, emended generic diagnosis, and oncomiracidium. Journal of Parasitology, 81, 616–625. DOI: 10.2307/3283862

    Article  CAS  Google Scholar 

  • Bonham K., Guberlet J.E. 1938. Ectoparasitic trematodes of Puget Sound fishes. Acanthocotyle. American Midland Naturalist, 20, 590–602. DOI: 10.2307/2420295

    Article  Google Scholar 

  • Bullard S.A., Payne R.R., Braswell J.S. 2004. New genus with two new species of capsalid monogeneans from dasyatids in the Gulf of California. Journal of Parasitology, 90, 1412–1427. DOI: 10.1645/GE-304R

    Article  Google Scholar 

  • Bychowsky B.E. 1957. Monogenetic Trematodes, their Classification and Phylogeny. Academy of Sciences, U.S.S.R., Moscow, Leningrad

    Google Scholar 

  • Bychowsky B.E., Nagibina L.F. 1976. [New species of Monogenea of the genus Telegamatrix] (in Russian). Biologiya Morya, 2, 10–15

    Google Scholar 

  • Chisholm L.A., Whittington I.D. 1995. A revision of Dendromono-cotyle 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. DOI: 10.1080/00222939500770461

    Article  Google Scholar 

  • Chisholm L.A., Whittington I.D. 1996. A revision of Heterocotyle (Monogenea: Monocotylidae) with a description of Hetero-cotyle capricornensis n. sp. from Himantura fai (Dasyatidi-dae) from Heron Island, Great Barrier Reef, Australia. International Journal for Parasitology, 26, 1169–1190. DOI: 10.1016/S0020-7519(96)00113-0

    Article  CAS  Google Scholar 

  • Chisholm L.A., Whittington I.D. 1997. A revision of Neoheterocotyle (Monogenea: Monocotylidae) with descriptions of the larvae of N. rhinobatis and N. rhynchobatis from Heron Island, Great Barrier Reef, Australia. International Journal for Parasitol-ogy, 27, 1041–1060. DOI: 10.1016/S0020-7519(97)00072-6

    Article  CAS  Google Scholar 

  • Combes C. 1968. Biologie, écologie des cycles et biogéographie de digènes et monogènes d’amphibiens dans l’est des Pyrénées. Mémoires du Muséum National d’Histoire Naturelle, Série A, Zoologie, 51, 1–195

    Google Scholar 

  • Deveney M.R., Whittington I.D. 2010. Three new species of Benedenia Diesing, 1858 from the Great Barrier Reef, Australia with a key to species of the genus. Zootaxa, 2348, 1–22

    Article  Google Scholar 

  • Dinh Hoai T., Hutson K.S. 2014. Reproductive strategies of the insidious fish ectoparasite, Neobenedenia sp. (Capsalidae: Monogenea). PLoS ONE, 9, 1–7. e108801. DOI: 10.1371/journal.pone.0108801

    Article  CAS  Google Scholar 

  • Dollfus R.P., Euzet, L. 1973. Nouvelles données sur Paracyclocotyla cherbonnieri Dollfus, 1970 (Monogenea). Bulletin du Muséum National d’Histoire Naturelle, Zoologie, 101, 815–819

    Google Scholar 

  • El-Naggar M.M., El-Naggar A.A., Kearn G.C. 2004. Swimming in Gyrodactylus rysavyi (Monogenea, Gyrodactylidae) from the Nile catfish, Clarias gariepinus. Acta Parasitologica, 49, 102–107

    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. DOI: 10.1016/S0020-7519(83) 80067-8

    Article  Google Scholar 

  • Euzet L., Cauwet A. 1967. Polylabris diplodi n. g., n. sp. (Monogenea, Microcotylidae) parasite de téléostéens du genre Diplodus (Sparidae). Bulletin du Muséum National d’Histoire Naturelle, 39, 213–220

    Google Scholar 

  • Euzet L., Ktari M.H. 1970a. Pyragraphorus hollisae sp. nov. (Monogenea) parasite de Lichia glauca (L., 1758) (Carangidae) en Méditerranée. Anales del Instituto de Biologia, Universidad Nacional Autonoma de Mexico, 41, 6–72

    Google Scholar 

  • Euzet L., Ktari M.H. 1970b. Heteraxinoides hannibali n.sp. (Monogenea, Polyopisthocotylea), parasite branchial de Pomadasys incisus (Bowdich, 1825) (Teleostei) dans le Golfe de Tunis. Bulletin du Muséum National d’Histoire Naturelle, 41, 269–279

    Google Scholar 

  • Euzet L., Ktari M.H. 1971. Aspinatrium gallieni n. sp. (Monogenea, Polyopisthocotylea) parasite de Strongylura acus Lacépède, 1803 en Méditerranée. Bulletin de la Société Zoologique de France, 96, 509–517

    Google Scholar 

  • Euzet L., Maillard C. 1973. Sur deux Microcotylidae (Monogenea) parasites branchiaux de téléostéens du genre Diplodus (Spari-dae). Bulletin du Muséum National d’Histoire Naturelle, Zoologie, 101, 793–805

    Google Scholar 

  • Euzet L., Suriano D.M. 1977. Ligophorus n.g. (Monogenea, Ancy-rocephalidae) parasite des Mugilidae (téléostéens) en Méditerranée. Bulletin du Muséum National d’Histoire Naturelle, Zoologie, 329, 799–822

    Google Scholar 

  • Euzet L., Wahl E. 1977. Bicotylophora baeri n. sp. (Monogenea) parasite branchial du téléostéen Trachinotus falcatus (L., 1758) en Côte-d’Ivoire. Revue Suisse de Zoologie, 84, 71–79

    Article  CAS  Google Scholar 

  • Gusev A.V. 1985. Class Monogenea. In: (Ed. O.N. Bauer) Keys to Parasites of the Freshwater Fish Fauna of the USSR. Vol. 2. Parasitic Metazoa. Leningrad Publishing House “Nauka”, Leningrad. 425 pp. (In Russian)

    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. DOI: 10.2307/3283449

    Article  CAS  Google Scholar 

  • Justine J-L. 1995. Spermatozoal ultrastructure and phylogeny in the parasitic platyhelminthes. In: Jamieson B.G.M., Ausio J., Justine J-L. (eds), Advances in Spermatozoal Phylogeny and Taxonomy. Mémoires du Muséum National d’Histoire Naturelle, 166, 55–86

    Google Scholar 

  • Justine J-L., Le Brun N., Mattei X. 1985. The aflagellate spermatozoon of Diplozoon (Platyhelminthes: Monogenea: Polyopisthocotylea): a demonstrative case of relationship between sperm ultrastructure and biology of reproduction. Journal of Ultrastructure Research, 92, 47–54. DOI: 10.1016/0889-1605(85)90126-0

    Article  CAS  Google Scholar 

  • Kearn G.C. 1965. The biology of Leptocotyle minor, a skin parasite of the dogfish, Scyliorhinus canicula. Parasitology, 55, 473–480. DOI: 10.1017/S0031182000069183

    Article  Google Scholar 

  • Kearn G.C. 1970. The production, transfer and assimilation of sper-matophores by Entobdella soleae, a monogenean skin parasite of the common sole. Parasitology, 60, 301–311. DOI: 10.1017/S0031182000078136

    Article  CAS  Google Scholar 

  • Kearn G.C. 1984. The migration of the monogenean Entobdella soleae on the surface of its host, Solea solea. International Journal for Parasitology, 14, 63–69. DOI: 10.1016/0020-7519(84)90013-4

    Article  Google Scholar 

  • Kearn G.C. 1986. The eggs of monogeneans. Advances in Parasitology, 25, 175–273. DOI: 10.1016/S0065-308X(08)60344-9

    Article  CAS  Google Scholar 

  • Kearn G.C. 1988. The monogenean skin parasite Entobdella soleae: movement of adults and juveniles from host to host (Solea solea). International Journal for Parasitology, 18, 313–319. DOI: 10.1016/0020-7519(88)90139-7

    Article  CAS  Google Scholar 

  • Kearn G.C. 1992. Mating in the capsalid monogenean Benedenia seriolae, a skin parasite of the yellowtail, Seriola quinqueradiata in Japan. Publications of the Seto Marine Biological Laboratory, 35, 273–280

    Article  Google Scholar 

  • Kearn G.C. 1994. Evolutionary expansion of the Monogenea. International Journal for Parasitology, 24, 1227–1271. DOI: 10.1016/0020-7519(94)90193-7

    Article  CAS  Google Scholar 

  • Kearn G.C. 1998. Parasitism and the Platyhelminths. Chapman & Hall, London. 544 pp.

    Google Scholar 

  • Kearn G.C. 2004. Leeches, Lice and Lampreys. A Natural History of Skin and Gill Parasites of Fishes. Springer, The Netherlands. pp. 432

    Google Scholar 

  • Kearn, G.C. 2006. Sub-tegumental ventral fibres surrounding the vaginal opening of Entobdella soleae (van Beneden et Hesse, 1864) Johnston, 1929 (Platyhelminthes: Monogenea: Capsal-idae). Folia Parasitologica, 53, 71–72. DOI: 10.14411/fp. 2006.007

    Article  Google Scholar 

  • Kearn G.C., James R., Evans-Gowing R. 1993. Insemination and population density in Entobdella soleae, a monogenean skin parasite of the common sole, Solea solea. International Journal for Parasitology, 23, 891–899. DOI: 10.1016/0020-7519(93)90055-4

    Article  CAS  Google Scholar 

  • Kearn G.C., Whittington I.D. 1991. Swimming in a sub-adult mono-genean of the genus Entobdella. International Journal for Parasitology, 21, 739–741. DOI: 10.1016/0020-7519(91) 90090-T

    Article  CAS  Google Scholar 

  • Kearn G.C., Whittington I.D. 1992. Diversity of reproductive behaviour in platyhelminth parasites: insemination in some benedeniine (capsalid) monogeneans. Parasitology, 104, 489–496. DOI: 10.1017/S0031182000063757

    Article  Google Scholar 

  • Kearn G.C., Whittington I.D. 1994. Ancyrocephaline monogeneans of the genera Chauhanellus and Hamatopeduncularia from the gills of the blue catfish, Arius graeffei, in the Brisbane River and Moreton Bay, Queensland, Australia, with descriptions of four new species. International Journal for Parasitology, 24, 569–588. DOI: 10.1016/0020-7519(94)90149-X

    Article  CAS  Google Scholar 

  • Kearn G.C., Whittington I.D. 2005. Neoentobdella gen. nov. for species of Entobdella Blainville in Lamarck, 1818 (Monogenea, Capsalidae, Entobdellinae) from stingray hosts, with descriptions of two new species. Acta Parasitologica, 50, 32–48

    Google Scholar 

  • Kearn G.C., Whittington I.D., Euzet L. 2006. The handling and fate of spermatophores in Neoentobdella diadema and N. apiocolpos (Monogenea: Capsalidae: Entobdellinae). Folia Parasitologica, 53, 57–62. DOI: 10.14411/fp.2006.005

    Article  Google Scholar 

  • Kearn G.C., Whittington I.D., Evans-Gowing R. 2010. A new genus and new species of microbothriid monogenean (Platyhelminthes) with a functionally enigmatic reproductive system, parasitic on the skin and mouth lining of the largetooth sawfish, Pristis microdon, in Australia. Acta Parasitologica, 55, 115–122. DOI: 10.2478/s11686-010-0019-1

    Article  Google Scholar 

  • Kearn G.C., Whittington I.D., Evans-Gowing R. 2011. Spermatophores in Dermopristis cairae Whittington et Kearn, 2011 (Monogenea, Microbothriidae). Acta Parasitologica, 56, 371–376

    Article  Google Scholar 

  • Lambert M., Euzet L. 1979. Espèces nouvelles du genre Cynoscioni-cola Price, 1962 (Monogenea, Microcotylidae). Zeitschrift für Parasitenkunde, 60, 229–237. DOI: 10.1007/BF0092 9170

    Article  Google Scholar 

  • Llewellyn J. 1956. The host-specificity, microecology, adhesive attitudes, and comparative morphology of some trematode gill parasites. Journal of the Marine Biological Association of the United Kingdom, 35, 113–127. DOI: 10.1017/S002531540 0009000

    Article  Google Scholar 

  • Llewellyn J. 1960. Amphibdellid (monogenean) parasites of electric rays (Torpedinidae). Journal of the Marine Biological Association of the United Kingdom, 39, 561–589. DOI: 10.1017/S0025315400013552

    Article  Google Scholar 

  • Llewellyn J. 1983. Sperm transfer in the monogenean gill parasite Gastrocotyle trachuri. Proceedings of the Royal Society of London, B, 219, 439–446. DOI: 10.1098/rspb.1983.0083

    Article  Google Scholar 

  • Llewellyn J., Anderson M. 1984. The functional morphology of the copulatory apparatus of Ergenstrema labrosi and Ligophorus angustus, monogenean gill parasites of Chelon labrosus. Parasitology, 88, 1–7. DOI: 10.1017/S003118200 0054287

    Article  Google Scholar 

  • Llewellyn J., Euzet L. 1964. Spermatophores in the monogenean Entobdella diadema Monticelli from the skin of stingrays, with a note on the taxonomy of the parasite. Parasitology, 54, 337–344. DOI: 10.1017/S0031182000067962

    Article  Google Scholar 

  • MacCallum G.A. 1913. Fertilization and egglaying in Microcotyle stenotomi. Science, 37, 340–341. DOI: 10.1126/science.37. 948.340

    Article  CAS  Google Scholar 

  • Macdonald S., Caley J. 1975. Sexual reproduction in the monoge-nean Diclidophora merlangi: tissue penetration by sperms. Zeitschrift für Parasitenkunde, 45, 323–334. DOI: 10.1007/BF00329822

    Article  CAS  Google Scholar 

  • Macdonald S., Llewellyn J. 1980. Reproduction in Acanthocotyle greeni n. sp. (Monogenea) from the skin of Raia spp. at Plymouth. Journal of the Marine Biological Association of the United Kingdom, 60, 81–88. DOI: 10.1017/S0025315400 024139

    Article  Google Scholar 

  • Nollen P.M. 1978. Studies on the reproductive system of Philoph-thalmus gralli using techniques of transplantation and autoradiography. Journal of Parasitology, 64, 613–616. DOI: 10.2307/3279944

    Article  CAS  Google Scholar 

  • Nollen P.M. 1984. Mating behavior of Philophthalmus megalurus and P. gralli concurrent infections of chicks. International Journal for Parasitology, 14, 71–74. DOI: 10.1016/0020-7519(84)90014-6

    Article  Google Scholar 

  • Nollen P.M. 1990. Echinostoma caproni: Mating behavior and the timing of development and movement of reproductive cells. Journal of Parasitology, 76, 784–789. DOI: 10.2307/3282795

    Article  CAS  Google Scholar 

  • Ogawa K., Shirakashi S., Ishitani H. 2014. Insemination of the monogenean Neobenedenia girellae (Capsalidae, Benedeniinae). Parasitology International, 63, 473–478. DOI: 10.1016/j.parint. 2013.10.009

    Article  CAS  Google Scholar 

  • Oliver G. 1968. Recherches sur les Diplectanidae (Monogenea) parasites de téléostéens du Golfe du Lion. 1. -Diplectaninae Monticelli, 1903. Vie et Milieu, Série A: Biologie Marine, 19, 95–138

    Google Scholar 

  • Oliver G. 1969. Recherches sur les Diplectanidae (Monogenea) parasites de téléostéens du Golfe du Lion. III. Biologie. Vie et Milieu, Série A: Biologie Marine, 20, 397–420

    Google Scholar 

  • Oliver G. 1987. Les Diplectanidae Bychowsky, 1957 (Monogenea, Monopisthocotylea, Dactylogyridea). Systématique. Biologie. Ontogénie. Ecologie. Essai de Phylogenèse. Thesis. Académie de Montpellier. Université des Sciences et Techniques du Languedoc, France

    Google Scholar 

  • Paling J.E. 1966. The functional morphology of the genitalia of the spermatophore-producing monogenean parasite Diplectanum aequans (Wagener) Diesing, with a note on the copulation of the parasite. Parasitology, 56, 367–383. DOI: 10.1017/S003 1182000070979

    Article  CAS  Google Scholar 

  • Silan P. 1984. Biologie comparé des populations de Diplectanum ae-quans et Diplectanum laubieri, monogènes branchiaux de Dicentrarchus labrax. Thesis. Montpellier. Université des Sciences et Techniques du Languedoc

    Google Scholar 

  • Silan P., Euzet L., Maillard C. 1983. La reproduction chez Diplectanum aequans (Monogenea, Monopisthocotylea). Nouvelles données sur l’anatomie du complexe génital et son fonctionnement. Bulletin de la Société Française de Parasitologie, 1, 31–36

    Google Scholar 

  • Whittington I.D. 1990. Empruthotrema kearni n. sp. and observations on Thaumatocotyle pseudodasybatis Hargis, 1955 (Monogenea: Monocotylidae) from the nasal fossae of Aetobatus narinari (Batiformes: Myliobatidae). from Moreton Bay, Queensland. Systematic Parasitology, 15, 23–31. DOI: 10.1007/BF00009915

    Article  Google Scholar 

  • Whittington I.D. 2010. Revision of Benedeniella Johnston, 1929 (Monogenea: Capsalidae), its assignment to Entobdellinae Bychowsky, 1957 and comments on subfamilial composition. Zootaxa, 2519, 1–30

    Article  Google Scholar 

  • Whittington I.D., Ernst I. 2002. Migration, site-specificity and development of Benedenia lutjani (Monogenea: Capsalidae) on the surface of its host, Lutjanus carponotatus (Pisces: Lutjanidae). Parasitology, 124, 423–434. DOI: 10.1017/S003 1182001001287

    Article  CAS  Google Scholar 

  • 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. DOI: 10.1080/00 222939600770611

    Article  Google 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. DOI: 10.1080/00222939300770011

    Article  Google Scholar 

  • Whittington I.D., Kearn G.C. 2008. Trimusculotrema heronensis sp. nov. (Monogenea, Capsalidae) from the skin of the pink whipray Himantura fai (Elasmobranchii, Dasyatidae) from Heron Island, Queensland, Australia. Acta Parasitologica, 53, 251–257. DOI:10.2478/s11686-008-0044-5

    Article  Google Scholar 

  • Whittington I.D., Kearn G.C. 2009a. Two new species of entobdelline skin parasites (Monogenea, Capsalidae) from the blotched fan-tail ray, Taeniura meyeni, in the Pacific Ocean, with comments on spermatophores and the male copulatory apparatus. Acta Parasitologica, 54, 12–21. DOI: 10.2478/s11686-009-0013-7

    Article  Google Scholar 

  • Whittington I.D., Kearn G.C. 2009b. Two new species of Neoentob-della (Monogenea: Capsalidae: Entobdellinae) from the skin of Australian stingrays (Dasyatidae). Folia Parasitologica, 56, 29–35. DOI: 10.14411/fp.2009.005

    Article  Google Scholar 

  • Whittington I.D., Kearn G.C., Beverley-Burton M. 1994. Benedenia rohdei n. sp. (Monogenea: Capsalidae) from the gills of Lutjanus carponotatus (Perciformes: Lutjanidae) from the Great Barrier Reef, Queensland, Australia, with a description of the oncomiracidium. Systematic Parasitology, 28, 5–13. DOI: 10.1007/BF00006905

    Article  Google Scholar 

  • Winch J. 1983. The biology of Atrispinum labracis n. comb. (Monogenea) on the gills of the bass, Dicentrachus labrax. Journal of the Marine Biological Association of the United Kingdom, 63, 915–927. DOI: 10.1017/S0025315400071320

    Article  Google Scholar 

  • Zeller E. 1876. Weiterer Beitrag zur Kenntniss der Polystomen. Zeitschrift für Parasitenkunde, Zoologie, 27, 238–274

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Graham Kearn.

Additional information

Deceased.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kearn, G., Whittington, I. Sperm transfer in monogenean (platyhelminth) parasites. Acta Parasit. 60, 567–600 (2015). https://doi.org/10.1515/ap-2015-0082

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/ap-2015-0082

Keywords

Navigation