Architecture of haptoral musculature in three species of Ligophorus (Monogenea, Ancyrocephalidae)

A.A. Petrov, M.P. Popyuk, E.V. Dmitrieva and P.I. Gerasev

Proceedings of the Zoological Institute RAS, 2015, 319(2): 244–256 · https://doi.org/10.31610/trudyzin/2015.319.2.244

Full text

Abstract

The posterior attachment organs of monogeneans known as haptors show exceptional morphological plasticity and play a major role in monogenean taxonomy. Our knowledge of haptoral musculature, however, is still very limited and further study of this musculature in different groups of monogeneans may be instrumental in improving their taxonomic system and furthering our knowledge of their modes of attachment. This study used phalloidin staining in conjunction with confocal microscopy to examine haptoral musculature in three species of Ligophorus (L. llewelyni Dmitrieva et al., 2007, L. pilengas Sarabeev et Balbuena, 2004 and L. kaohsianghsieni (Gusev, 1962) Gusev, 1985), a member of the monopisthocotylean family Ancyrocephalidae sensu Bychovsky et Nagibina, 1978. Sclerotised structures (anchors, connecting bars and marginal hooks) were visualised simultaneously with muscles by capturing laser light reflected off the surfaces of these sclerites. The haptoral musculature was shown to be identical in L. pilengas and L. llewelyni and essentially similar between these two species and L. kaohsianghsieni, but the latter species had also some notable differences. Common to all three species were thick extrinsic muscles arising from the inner roots of the anchors, a muscle bundle connecting the inner roots of the opposite ventral anchors, muscles running from the outer roots of the anchors to the body wall, muscles originating from the dorsal bar and inserting on the anchoral openings and muscles connecting the bars with anchoral roots. Ligophorus llewelyni and L. pilengas have a more elaborate haptoral musculature than L. kaohsianghsieni with some additional muscles, tendon-like muscle extensions and a strong bracket-shaped muscle presumably functioning as a catch-muscle for the dorsal anchors. Functional roles of individual haptoral muscles in attachment are discussed and the architecture of haptoral musculature in Ligophorus is compared with that of other ancyrocephalids.

Key words

confocal microscopy, haptor, Ligophorus, Monogenea, musculature, phalloidin staining

Submitted March 11, 2015 · Accepted April 15, 2015 · Published June 25, 2015

References

Arafa S.Z. 2011. Ultrastructure of musculature of the marginal hooklets of Macrogyrodactylus congolensis, a monogenean skin parasite from the catfish Clarias gariepinus. Acta Parasitologica, 56: 122–130. https://doi.org/10.2478/s11686-011-0020-3

Arafa S.Z., El-Naggar M.M., El-Abbassy S.A., Stewart M.T. and Halton D.W. 2007. Neuromusculature of Gyrodactylus rysavyi, a monogenean gill and skin parasite of the catfish Clarias gariepinus. Parasitology International, 56: 297–307. https://doi.org/10.1016/j.parint.2007.06.005

Blasco-Costa I., Míguez-Lozano R., Sarabeev V. and Balbuena J.A. 2012. Molecular phylogeny of species of Ligophorus (Monogenea: Dactylogyridae) and their affinities within the Dactylogyridae. Parasitology International, 61: 619–627. https://doi.org/10.1016/j.parint.2012.06.004

Bychovsky B.E. and Nagibina L.F. 1968. Triacanthinella, a new genus of marine monogenean parasites of hornfishes. Parazitologiya, 2: 148–158. [In Russian].

El-Naggar M., Arafa S., El-Abbassy S., Stewart M. and Halton D. 2004. Neuromusculature of Macrogyrodactylus clarii, a monogenean gill parasite of the Nile catfish Clarias gariepinus in Egypt. Parasitology Research, 94: 163–175. https://doi.org/10.1007/s00436-004-1198-1

El-Naggar M., Arafa S., El-Abbassy S., Stewart M. and Halton D. 2007. Neuromusculature of Macrogyrodactylus congolensis, a monogenean skin parasite of the Nile catfish Clarias gariepinus. Parasitology Research, 100: 265–279. https://doi.org/10.1007/s00436-006-0235-7

Garcia-Vasquez A., Shinn A. and Bron J. 2012. Development of a light microscopy stain for the sclerites of Gyrodactylus von Nordmann, 1832 (Monogenea) and related genera. Parasitology Research, 110: 1639–1648. https://doi.org/10.1007/s00436-011-2675-y

Gerasev P.I. 1977. The mechanism of attachment to the host’s gills in Dactylogyrus extensus and D. achmerowi (Monogenoidea). Parazitologiya, 11: 513–519. [In Russian].

Gerasev P.I. 1981. Muscular systems of haptors and the attachment mechanism of some species of Dactylogyrus (Monogenea, Dactylogyridae). Parasitologicheskiy sbornik, 30: 190–205. [In Russian].

Gerasev P.I. 1989. Major muscles of hamuli in Amuro-Chinese Dactylogyrus (Monogenoidea). Parazitologicheskiye issledovaniya. DVO AN SSSR, Vladivostok: 39–45. [In Russian].

Gerasev P.I. 1998. The family Tetraonchidae (Monogenea): structure and position among monogeneans. Parazitologiya, 32: 544–552. [In Russian].

Halton D. and Maule A. 2004. Flatworm nerve-muscle: structural and functional analysis. Canadian Journal of Zoology, 82: 316–333. https://doi.org/10.1139/z03-221

Halton D.W., Maule A.G., Mair G.R. and Shaw C. 1998. Monogenean neuromusculature: some structural and functional correlates. International Journal for Parasitology, 28: 1609–1623. https://doi.org/10.1016/S0020-7519(98)00063-0

Justine J.-L., Jovelin R., Neifar L., Mollaret I., Lim L.H.S., Hendrix S.S. and Euzet L. 2002. Phylogenetic positions of the Bothitrematidae and Neocalceostomatidae (Monopisthocotylean monogeneans) inferred from 28S rDNA sequences. Comparative Parasitology, 69: 20–25. https://doi.org/10.1654/1525-2647(2002)069[0020:PPOTBA]2.0.CO;2

Kearn G. 1966. The adhesive mechanism of the monogenean parasite Tetraonchus monenteron from the gills of the pike (Esox lucius). Parasitology, 56: 505–510. https://doi.org/10.1017/S0031182000068980

Kearn G. 1971. The attachment of the ancyrocephalid monogenean Haliotrema balisticus to the gills of the trigger fish, Balistes capriscus (= carolinensis). Parasitology, 63: 157–162. https://doi.org/10.1017/S0031182000067500

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

Plaisance L., Littlewood D.T.J., Olson P.D. and Morand S. 2005. Molecular phylogeny of gill monogeneans (Platyhelmintes, Monogenea, Dactylogyridae) and colonization of Indo-West West Pacific butterflyfish hosts (Perciformes, Chaetodontidae). Zoologica Scripta, 34: 425–436. https://doi.org/10.1111/j.1463-6409.2005.00191.x

Pronkina N.V., Dmitrieva E.V., Gerasev P.I. and Gibson D.I. 2013. The distribution of species of Ligophorus Euzet et Suriano, 1977 (Ancyrocephalidae) on the gills of their hosts: coexistence and species divergence. Abstracts of 7th International Symposium on Monogenea, August 4–9, 2013. Rio de Janeiro: 81. https://doi.org/10.1007/s11230-011-9341-8

Sarabeev V. and Desdevises Y. 2014. Phylogeny of the Atlantic and Pacific species of Ligophorus (Monogenea: Dactylogyridae): Morphology vs. molecules. Parasitology International, 63: 9–20. https://doi.org/10.1016/j.parint.2013.10.001

Šimková A., Matejusová I. and Cunningham C.O. 2006. A molecular phylogeny of the Dactylogyridae sensu Kritsky and Boeger (1989) (Monogenea) based on the D1–D3 domains of large subunit rDNA. Parasitology, 133: 43–53. https://doi.org/10.1017/S0031182006009942

Šimková A., Plaisance L., Matějusová I., Morand S. and Verneau O. 2003. Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Systematic Parasitology, 54: 1–11. https://doi.org/10.1023/A:1022133608662

Valigurová A., Hodová I., Sonnek R., Koubková B. and Gelnar M. 2011. Eudiplozoon nipponicum in focus: monogenean exhibiting a highly specialized adaptation for ectoparasitic lifestyle. Parasitology Research, 108: 383–394. https://doi.org/10.1007/s00436-010-2077-6

Zurawski T., Mousley A., Mair G., Brennan G., Maule A., Gelnar M. and Halton D. 2001. Immunomicroscopical observations on the nervous system of adult Eudiplozoon nipponicum (Monogenea: Diplozoidae). International Journal for Parasitology, 31: 783–792. https://doi.org/10.1016/S0020-7519(01)00192-8

Zurawski T., Mousley A., Maule A., Gelnar M. and Halton D. 2003. Cytochemical studies of the neuromuscular systems of the diporpa and juvenile stages of Eudiplozoon nipponicum (Monogenea: Diplozoidae). Parasitology, 126: 349–357. https://doi.org/10.1017/S0031182002002871