Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-19T23:57:15.413Z Has data issue: false hasContentIssue false

Neuromuscular organization and haptoral armament of Polyclithrum ponticum (Monogenea: Gyrodactylidae)

Published online by Cambridge University Press:  13 October 2022

A. A. Petrov*
Affiliation:
Zoological Institute, Saint-Petersburg, Russia
E. V. Dmitrieva
Affiliation:
A.O. Kovalevsky Institute of Biology of the Southern Seas, Moscow, Russia
M. P. Plaksina
Affiliation:
Murmansk Marine Biological Institute, Murmansk, Russia
*
Author for correspondence: Anatoly A. Petrov, E-mail: [email protected]

Abstract

Most gyrodactylids have a haptor armed with a pair of hamuli, two connecting bars and 16 marginal hooks. In some gyrodactylids, however, the haptor is disc-shaped and reinforced by additional sclerites. The genus Polyclithrum has arguably the most elaborate haptor in this group. This study aimed to gain better understanding of the anatomy of Polyclithrum by examining neuromusculature and haptoral armament of Polyclithrum ponticum, a species parasitizing Mugil cephalus in the Black Sea, with emphasis on haptoral sclerites and musculature in connection with host-attachment mechanisms. Musculature was stained by phalloidin, the nervous system by anti-serotonin and anti-FMRFamide antibodies, and haptoral sclerites were visualized in reflected light. The study provided new information on sclerites: in addition to previously described supplementary sclerites (A1–6), ear-shaped sclerites (ESSs) and two paired groups of ribs, reflected light revealed a rod-shaped process on the ESSs and a pair of small posterior sclerites. The sclerites were shown to be operated by 16 muscles, the most prominent of which were two transverse muscles connecting the hamular roots, three muscles attached to sclerite A2, the muscle fibres of anterior ribs and a set of extrinsic muscles. The nervous system consists of a pair of cerebral ganglia connected by a commissure and three pairs of nerve cords that unite in the haptor to form a loop between the opposite cords. The arrangement of sclerites and muscles suggests that Polyclithrum initiates the attachment by clamping a host's surface with longitudinally folded haptor and then secures its position with marginal hooks.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Arafa, SZ (2011) Ultrastructure of musculature of the marginal hooklets of Macrogyrodactylus congolensis, a monogenean skin parasite from the catfish Clarias gariepinus. Acta Parasitologica 56(2), 122130.CrossRefGoogle Scholar
Arafa, SZ, El-Naggar, MM and Kearn, GC (2003) Scanning electron microscope observations on the monogenean skin parasite Macrogyrodactylus congolensis (Prudhoe, 1957) Yamaguti, 1963. Acta Parasitologica 48(3), 163171.Google Scholar
Arafa, SZ, El-Naggar, MM, El-Abbassy, SA, Stewart, MT and Halton, DW (2007) Neuromusculature of Gyrodactylus rysavyi, a monogenean gill and skin parasite of the catfish Clarias gariepinus. Parasitology International 56(4), 297307.CrossRefGoogle ScholarPubMed
Arafa, SZ, El-Naggar, MM and El-Abbassy, AS (2009) Mode of attachment and histopathological effects of Macrogyrodactylus clarii, a monogenean gill parasite of the catfish Clarias gariepinus, with a report on host response. Acta Parasitologica 54(2), 103112.CrossRefGoogle Scholar
Arafa, SZ, El-Naggar, MM and Kearn, GC (2013) Ultrastructure of the digestive system and experimental study of feeding in the monogenean skin and fin parasite Macrogyrodactylus congolensis. Acta Parasitologica 58(4), 420433.CrossRefGoogle ScholarPubMed
Bakke, TA, Cable, J and Harris, PD (2007) The biology of gyrodactylid monogeneans: The “Russian-doll killers”. pp. 161376 in Baker, JR, Muller, R and Rollinson, D (Eds) Advances in parasitology, Vol. 64, Amsterdam, Academic Press.Google Scholar
Bakke, TA, Nilsen, BK and Shinn, PA (2004) Chaetotaxy applied to Norwegian Gyrodactylus salaris Malmberg, 1957 (Monogenea) clades and related species from salmonids. Folia Parasitologica 51(2–3), 253261.CrossRefGoogle ScholarPubMed
Boeger, WA, Kritsky, DC and Pie, MR (2003) Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zoologica Scripta 32(5), 437448.CrossRefGoogle Scholar
Boeger, WA, Kritsky, DC, Patella, L and Bueno-Silva, M (2021) Phylogenetic status and historical origins of the oviparous and viviparous gyrodactylids (Monogenoidea, Gyrodactylidea). Zoologica Scripta 50(1), 112124.CrossRefGoogle Scholar
Braun, F (1966) Beiträge zur mikroskopischen Anatomie und Fortpflanzungsbiologie von Gyrodactylus wageneri v. Nordmann, 1832 [Contributions to the microscopic anatomy and reproductive biology of Gyrodactylus wageneri v. Northman, 1832]. Zeitschrift für Parasitenkunde 28(2), 142174.CrossRefGoogle Scholar
Cable, J, Marks, NJ, Halton, DW, Shaw, C, Johnston, CF, Tinsley, RC and Gannicott, AM (1996) Cholinergic, serotoninergic and peptidergic components of the nervous system of Discocotyle sagittata (Monogenea: Polyopisthocotylea). International Journal for Parasitology 26(12), 13571367.CrossRefGoogle Scholar
Cone, DK and Odense, PH (1988) Light and scanning electron microscope studies of Fundulotrema prolongis (Monogenea: Gyrodactylidea) parasitizing Fundulus diaphanus (Cyprinodontidae) in Nova Scotia, Canada, with an emended diagnosis of Fundulotrema. Proceedings of the Helminthological Society of Washington 55(2), 224228.Google Scholar
Egger, B, Lapraz, F, Tomiczek, B, et al. (2015) A transcriptomic–phylogenomic analysis of the evolutionary relationships of flatworms. Current Biology 25(10), 13471353.CrossRefGoogle ScholarPubMed
Ehlers, U (1985) Das phylogenetische system der Plathelminthes [The phylogenetic system of Plathelminthes]. Stuttgart, New York, Gustav Fischer. [In German.]Google Scholar
El-Naggar, MM (2001) Microhabitat and movement of the viviparous monogeneans Gyrodactylus alberti, Macrogyrodactylus clarii and M. congolensis from the Nile catfish Clarias gariepinus. Journal of the Egyptian–German Society of Zoology 35(4), 169187.Google Scholar
El-Naggar, MM (2004) Swimming in Gyrodactylus rysavyi (Monogenea, Gyrodactylidae) from the Nile catfish, Clarias gariepinus. Acta Parasitologica 49(2), 102107.Google Scholar
El-Naggar, MM, Arafa, ZS, El-Abbassy, AS and Kearn, CG (2001) Chaetotaxy of the monogeneans Macrogyrodactylus clarii and M. congolensis from the gills and skin of the catfish Clarias gariepinus in Egypt, with a note on argentophilic elements in the nervous system. Folia Parasitologica 48(3), 201208.CrossRefGoogle Scholar
El-Naggar, MM, Arafa, SZ, El-Abbassy, SA, Stewart, MT and Halton, DW (2004) Neuromusculature of Macrogyrodactylus clarii, a monogenean gill parasite of the Nile catfish Clarias gariepinus in Egypt. Parasitology Research 94(3), 163175.CrossRefGoogle ScholarPubMed
El-Naggar, MM, Arafa, SZ, El-Abbassy, SA, Stewart, MT and Halton, DW (2007) Neuromusculature of Macrogyrodactylus congolensis, a monogenean skin parasite of the Nile catfish Clarias gariepinus. Parasitology Research 100(2), 265279.CrossRefGoogle ScholarPubMed
Ergens, R (1967) New species of the genus Gyrodacylus (Monogenoidea) from the Danube basin. Folia Parasitologica 14(4), 377379.Google Scholar
Ernst, I, Whittington, ID and Jones, MK (2000) Three new species of Polyclithrum Rogers, 1967 (Gyrodactylidae: Monogenea) from mugilid fishes from Australia and Brazil, with a redescription of P. mugilini Rogers, 1967. Systematic Parasitology 45(1), 6173.CrossRefGoogle ScholarPubMed
Fromm, B, Worren, MM, Hahn, C, Hovig, E and Bachmann, L (2013) Substantial loss of conserved and gain of novel microRNA families in flatworms. Molecular Biology and Evolution 30(12), 26192628.CrossRefGoogle ScholarPubMed
Gerasev, PI and Dmitrieva, EV (2005) The description of Gyrodactylus mulli sp. n. (Monogenea: Gyrodactylidae) from the Black Sea blunt-snouted mullet Mullus barbatus ponticus. Parazitologiya 39(4), 327331.Google Scholar
Gerasev, PI, Dmitrieva, EV and Gaevskaia, AV (2002) Policlithrum ponticum sp. n. (Monogenea: Gyrodactylidae: Polyclithrinae) from Mugil cephalus from the Black Sea and problems of suprageneric systematics of the gyrodactylids. Parazitologiya 36(5), 396404.Google Scholar
Grano-Maldonado, MI (2014) Ultrastructure of the external sensory apparatus of Gyrodactylus gasterostei Gläser, 1974. Microscopy Research and Technique 77(9), 740747.CrossRefGoogle ScholarPubMed
Grano-Maldonado, MI, de Sousa, CB and Rodríguez-Santiago, MA (2018) First insights into the ultrastructure of myosin and actin bands using transmission electron microscopy in Gyrodactylus (Mnogenea). The Journal of Microscopy and Ultrastructure 6(4), 177181.CrossRefGoogle Scholar
Halton, DW and Gustafsson, MKS (1996) Functional morphology of the platyhelminth nervous system. Parasitology 113(Suppl 1), 47–S72.CrossRefGoogle Scholar
Halton, DW and Maule, AG (2004) Flatworm nerve–muscle: structural and functional analysis. Canadian Journal of Zoology 82(2), 316333.CrossRefGoogle Scholar
Halton, DW, Maule, AG, Mair, GR and Shaw, C (1998) Monogenean neuromusculature: some structural and functional correlates. International Journal for Parasitology 28(10), 16091623.CrossRefGoogle ScholarPubMed
Hooge, MD (2001) Evolution of body-wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). Journal of Morphology 249(3), 171194.CrossRefGoogle Scholar
Jara, C, An, L and 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(2), 164166.Google Scholar
Krupenko, DY and Dobrovolskij, AA (2015) Somatic musculature in trematode hermaphroditic generation. BMC Evolutionary Biology 15(1), 128.CrossRefGoogle ScholarPubMed
Luus-Powell, JW, Mashego, NS and Khalil, FL (2003) Mormyrogyrodactylus gemini gen. et sp. n. (Monogenea: Gyrodactylidae), a new gyrodactylid from Marcusenius macrolepidotus (Mormyridae) from South Africa. Folia Parasitologica 50(1), 4955.CrossRefGoogle Scholar
Lyons, KM (1969) Compound sensilla in monogenean skin parasites. Parasitology 59(3), 625636.CrossRefGoogle Scholar
Lyons, KM (1973) The epidermis and sense organs of the Monogenea and some related groups. pp. 193232 in Dawes, B (Ed.) Advances in parasitology, Vol. 11, London and New York, Academic Press.Google Scholar
Mair, GR, Halton, DW and Maule, AG (2020) The neuromuscular system of the sheep tapeworm Moniezia expansa. Invertebrate Neuroscience 20(4), 17.CrossRefGoogle ScholarPubMed
Mair, GR, Maule, AG, Fried, B, Day, TA and Halton, DW (2003) Organization of the musculature of schistosome cercariae. Journal of Parasitology 89(3), 623625.CrossRefGoogle ScholarPubMed
Mair, GR, Maule, AG, Shaw, C, Johnston, CF and Halton, DW (1998) Gross anatomy of the muscle systems of Fasciola hepatica as visualized by phalloidin-fluorescence and confocal microscopy. Parasitology 117(1), 7582.CrossRefGoogle ScholarPubMed
Maule, AG, Halton, DW, Johnston, CF, Shaw, C and Fairweather, I (1990) The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite, Diclidophora merlangi: a cytochemical study. Parasitology 100(2), 255273.CrossRefGoogle ScholarPubMed
Mochalova, NV, Terenina, NB, Poddubnaya, LG, Yashin, VA, Kuchin, AV and Kreshchenko, ND (2019) First evidence of serotoninergic components in the nervous system of the monogenean Chimaericola leptogaster (Chimaericolidae, Polyopisthocotylea), a gill parasite of the relict holocephalan fish. Folia Parasitologica 66(2), 19.CrossRefGoogle Scholar
Nefedova, DA, Terenina, NB, Mochalova, NV, Poddubnaya, LG, Movsesyan, SO, Gordeev, II, Kuchin, AV and Kreshchenko, ND (2021) The neuromuscular system in flatworms: serotonin and FMRFamide immunoreactivities and musculature in Prodistomum alaskense (Digenea: Lepocreadiidae), an endemic fish parasite of the northwestern Pacific. Canadian Journal of Zoology 99(8), 689701.CrossRefGoogle Scholar
Park, J-K, Kim, K-H, Kang, S, Kim, W, Eom, KS and Littlewood, DTJ (2007) A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of Microcotyle sebastis (Monogenea: Platyhelminthes). BMC Evolutionary Biology 7(1), 1111.CrossRefGoogle Scholar
Perkins, EM, Donnellan, SC, Bertozzi, T and Whittington, ID (2010) Closing the mitochondrial circle on paraphyly of the Monogenea (Platyhelminthes) infers evolution in the diet of parasitic flatworms. International Journal for Parasitology 40(11), 12371245.CrossRefGoogle ScholarPubMed
Petrov, AA and Gerasev, PI (2019) Muscular arrangement and sclerite morphology in the haptor of Tetraonchus monenteron (Monogenea, Dactylogyridea). Acta Parasitologica 64(1), 138147.CrossRefGoogle Scholar
Petrov, AA and Podvyaznaya, IM (2016) Muscle architecture during the course of development of Diplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae) from cercariae to metacercariae. Journal of Helminthology 90(3), 321336.CrossRefGoogle ScholarPubMed
Petrov, AA, Dmitrieva, EV, Popyuk, MP, Gerasev, PI and Petrov, SA (2017) Musculoskeletal and nervous systems of the attachment organ in three species of Diplectanum (Monogenea: Dactylogyroidea). Folia Parasitologica 64, 022.CrossRefGoogle Scholar
Petrov, AA, Gerasev, PI, Popyuk, MP and Dmitrieva, EV (2016) Haptoral neuromusculature in two species of Dactylogyrus Diesing, 1850 (Monogenea: Dactylogyridae). Systematic Parasitology 93(4), 337354.CrossRefGoogle Scholar
Petrov, AA, Popyuk, MP, Dmitrieva, EV and Gerasev, PI (2015) Architecture of haptoral musculature in three species of Ligophorus (Monogenea, Ancyrocephalidae). Trudy Zoologicheskogo Instituta RAN 319(2), 244256.Google Scholar
Přikrylová, I, Barson, M and Shinn, PA (2021) Description of Tresuncinidactylus wilmienae gen. et sp. n. (Monogenea: Gyrodactylidae), from the gills of the bulldog, Marcusenius macrolepidotus (Peters) from Lake Kariba, Zimbabwe. Folia Parasitologica 68, 025.CrossRefGoogle Scholar
Přikrylová, I, Shinn, AP and Paladini, G (2017) Description of Citharodactylus gagei n. gen. et n. sp. (Monogenea: Gyrodactylidae) from the moon fish, Citharinus citharus (Geoffroy Saint-Hilaire), from Lake Turkana. Parasitology Research 116(1), 281292.CrossRefGoogle Scholar
Přikrylová, I, Vanhove, MPM, Janssens, SB, Billeter, PA and Huyse, T (2013) Tiny worms from a mighty continent: high diversity and new phylogenetic lineages of African monogeneans. Molecular Phylogenetics and Evolution 67(1), 4352.CrossRefGoogle ScholarPubMed
Prudhoe, S (1957) Trematoda. Exploration du Parc National de L'Upemba 48(1), 128.Google Scholar
Prudhoe, S and Hussey, CG (1977) Some parasitic worms in freshwater fishes and fish-predators from the Transvaal, South Africa. Zoologica Africana 12(1), 113147.CrossRefGoogle Scholar
Reuter, M (1987) Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system of Gyrodactylus salaris (Monogenea). Acta Zoologica 68(3), 187193.CrossRefGoogle Scholar
Ribeiro, P, El-Shehabi, F and Patocka, N (2005) Classical transmitters and their receptors in flatworms. Parasitology 131(Suppl S1), 19–S40.CrossRefGoogle ScholarPubMed
Rogers, WA (1967) Polyclithrum mugilini gen. et sp. n. (Gyrodactylidae: Polyclithrinae Subfam. n.) from Mugil cephalus L. Journal of Parasitology 53(2), 274276.CrossRefGoogle Scholar
Rozario, T and Newmark, PA (2015) A confocal microscopy-based atlas of tissue architecture in the tapeworm Hymenolepis diminuta. Experimental Parasitology 158(1), 3141.CrossRefGoogle ScholarPubMed
Shinn, AP, Bron, JE, Sommerville, C and Gibson, DI (2003) Comments on the mechanism of attachment in species of the monogenean genus Gyrodactylus. Invertebrate Biology 122(1), 111.CrossRefGoogle Scholar
Shinn, AP, Sommerville, C and Gibson, DI (1998) The application of chaetotaxy in the discrimination of Gyrodactylus salaris Malmberg, 1957 (Gyrodactylidae: Monogenea) from species of the genus parasitising British salmonids. International Journal for Parasitology 28(5), 805814.CrossRefGoogle ScholarPubMed
Skinner, R (1975) Parasites of the striped mullet, Mugil cephalus, from Biscayne Bay, Florida, with descriptions of a new genus and three new species of trematodes. Bulletin of Marine Science 25(3), 318345.Google Scholar
Tyler, S and Hooge, M (2004) Comparative morphology of the body wall in flatworms (Platyhelminthes). Canadian Journal of Zoology 82(2), 194210.CrossRefGoogle Scholar
Vanhove, MPM, Snoeks, JOS, Volckaert, FAM and Huyse, T (2011) First description of monogenean parasites in Lake Tanganyika: the cichlid Simochromis diagramma (Teleostei, Cichlidae) harbours a high diversity of Gyrodactylus species (Platyhelminthes, Monogenea). Parasitology 138(3), 364380.CrossRefGoogle Scholar
Watson, NA and Rohde, K (1994) Two new sensory receptors in Gyrodactylus sp. (Platyhelminthes, Monogenea, Monopisthocotylea). Parasitology Research 80(5), 442445.CrossRefGoogle Scholar
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(8), 783792.CrossRefGoogle Scholar
Zurawski, TH, Mousley, A, Maule, AG, Gelnar, M and Halton, DW (2003) Cytochemical studies of the neuromuscular systems of the diporpa and juvenile stages of Eudiplozoon nipponicum (Monogenea: Diplozoidae). Parasitology 126(4), 349357.CrossRefGoogle Scholar