Skip to main content

Advertisement

Log in

Neuromusculature of Macrogyrodactylus clarii, a monogenean gill parasite of the Nile catfish Clarias gariepinus in Egypt

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Phalloidin fluorescence technique, enzyme cytochemistry and immunocytochemistry in conjunction with confocal scanning laser microscopy have been used for the first time to describe the nervous and muscle systems of the viviparous monogenean gill parasite, Macrogyrodactylus clarii. The gross spatial arrangement of muscle and associated cholinergic, peptidergic and aminergic innervations has been examined. The central nervous system (CNS) consists of paired cerebral ganglia from which emanate three pairs of longitudinal ventral, lateral and dorsal nerve cords, connected at intervals by transverse connectives. The CNS is better developed ventrally than dorsally or laterally, and has the strongest reactivity for all neuroactive substances examined. Structural and functional correlates of the neuromusculature of the pharynx, haptor and reproductive tracts have been examined. Results implicate acetylcholine, FMRFamide-related peptides (FaRPs) and serotonin in sensory and motor function in this monogenean, although confirmatory physiological data are obviously required.

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.

Fig. 1
Fig. 2A–G
Fig. 3 A, B
Fig. 4
Fig. 5
Fig. 6
Fig. 7A–E
Fig. 8A–C

Similar content being viewed by others

References

  • Arafa SZ, Reda ES, El-Naggar MM (2002) Cholinergic components of the nervous system of the digenean parasites, Haplorchoides cahirinus and Acanthostomum absconditum from catfish Bagrus bayad in Egypt. Acta Parasitol 47:272–279

    Google Scholar 

  • Bahatanger A, Gupta A, Srivastava R (1980) Histological and histochemistry of the neuroendocrine components of Ceylonocotyle scoliocoelium (Digenea: Trematoda). Z Parasitenkd 64:77–84

    Google Scholar 

  • Buchmann K, Mellergaard S (1988) Histochemical demonstration of the inhibitory effect of Nuvan and Neguvon on cholinesterase activity in Pseudodactylogyrus anguillae (Monogenea). Acta Vet Scand 29:51–55

    CAS  PubMed  Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and function in the nervous system of invertebrates, vol I. WH Freeman, San Francisco

  • Cable J, Harris PD (2002) Gyrodactylid developmental biology: historical review, current status and future trends. Int J Parasitol 32:255–280

    Article  CAS  PubMed  Google Scholar 

  • Cable J, Harris PD, Tinsley RC (1996a) Ultrastructural adaptations for viviparity in the female reproductive system of gyrodactylid monogeneans. Tissue Cell 28:515–526

    Google Scholar 

  • Cable J, Marks NJ, Halton DW, Shaw C, Johnston CF, Tinsley RC, Gannicott AM (1996b) Cholinergic, serotoninergic and peptidergic components of the nervous system of Discocotyle sagittata (Monogenea: Polyopisthocotylea). Int J Parasitol 26:1357–1367

    Article  CAS  PubMed  Google Scholar 

  • Cable J, Harris PD, Tinsley RC (1998) Life history specializations of monogenean flatworms: a review of experimental and microscopical studies. Microsc Res Tech 42:186–199

    Article  CAS  PubMed  Google Scholar 

  • Coons AH, Leduc EH, Connelly JM (1955) Studies on antibody production. I. A method for histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. J Exp Med 102:42–60

    Article  Google Scholar 

  • Day TA, Maule AG (1999) Parasitic peptides! The structure and function of neuropeptides in parasitic worms. Peptides 20:999–1019

    Article  CAS  PubMed  Google Scholar 

  • El-Naggar MM (1993) Scanning electron microscope observations on the head lobes and haptor of the monogenean Macrogyrodactylus clarii Gussev, 1961. J Egyptian German Soc Zool 10:143–155

    Google Scholar 

  • El-Naggar MM, El-Abbassy SA (2003) Anatomical observations on the viviparous monogenean Gyrodactylus rysavyi Ergens, 1973 from the Nile catfish Clarias gariepinus in Egypt. Egyptian J Zool 40:225–249

    Google Scholar 

  • El-Naggar MM, Kearn GC (1980) Ultrastructural observations on the anterior adhesive apparatus in the monogeneans Dactylogyrus amphibothrium Wagener, 1857 and D. hemiamphibothrium Ergens 1956. Z Parasitenkd 61:223–241

    CAS  PubMed  Google Scholar 

  • El-Naggar MM, Serag HM (1986) Quadriacanthus aegypticus n sp., a monogenean gill parasite from the Egypt teleost Clarias lazera. Syst Parasitol 8:129–140

    Google Scholar 

  • El-Naggar MM, Serag HM (1987) Redescription of Macrogyrodactylus clarii Gussev 1961, a monogenean gill parasite of Clarias lazera in Egypt. Arab Gulf J Sci Res Agric Biol Sci 5:257–271

    Google Scholar 

  • El-Naggar MM, Kearn, GC, Hagras AE, Arafa SZ (1999) On some anatomical features of Macrogyrodactylus congolensis, a viviparous monogenean ectoparasite of the catfish Clarias gariepinus from Nile water. J Egyptian German Soc Zool 29:1–24

    Google Scholar 

  • El-Naggar MM, Arafa SZ, El-Abbassy SA, Kearn GC (2001a) 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 Parasitol 48:201–208

    CAS  PubMed  Google Scholar 

  • El-Naggar MM, El-Naggar AM, El-Abbassy SA (2001b) Microhabitat and movement of the viviparous monogeneans Gyrodactylus alberti, Macrogyrodactylus clarii and M. congolensis from the Nile catfish Clarias gariepinus. J Egyptian German Soc Zool Invertebr Zool Parasitol 35(D):169–187

    Google Scholar 

  • Gussev AV (1961) A viviparous monogenetic trematode from freshwater basins of Africa. Dokl Akad Nauka SSSR 136:490–493

    Google Scholar 

  • Halton DW, Gustafsson MKS (1996) Functional morphology of the platyhelminth nervous system. Parasitology 113:S57–S72

    Google Scholar 

  • Halton DW, Jennings JB (1964) Demonstration of the nervous system of the monogenetic trematode Diplozoon paradoxum Nordmann by the indoxyl acetate method for esterases. Nature 202:510–511

    CAS  PubMed  Google Scholar 

  • Halton DW, Morris GP (1969) Occurrence of cholinesterase and ciliated sensory structures in a fish gill fluke, Diclidophora merlangi (Trematoda: Monogenea). Z Parasitenkd 33:21–30

    Google Scholar 

  • Halton DW, Maule AG, Shaw C (1993) Neuronal mediators in monongenean parasites. Bull Fr Pêche Piscicult 328:82–104

    Google Scholar 

  • Halton DW, Maule AG, Mair GR, Shaw C (1998) Monogenean neuromusculature: some structural and functional correlates. Int J Parasitol 28:1609–1623

    Article  CAS  PubMed  Google Scholar 

  • Harris PD (1983) The morphology and life-cycle of the oviparous Gyrodactylus farlowellae gen. et sp. nov. (Monogenea Gyrodactyidae). Parasitology 87:405–420

    Google Scholar 

  • Kearn GC (1963) Feeding in some monogenean skin parasites: Entobdella solea on Solae solae and Acanthocotyle sp. on Raia clavata. J Biol Assoc UK 43:749–766

    Google Scholar 

  • Khalil LF (1970) Further studies on Macrogyrodactylus polypteri, a monogenean on the African freshwater fish Polypterus senegalus. J Helminthol 44:329–348

    Google Scholar 

  • Llewellyn J (1981) Evolution of viviparity and invasion by adults. Parasitology 82:64–66

    Google Scholar 

  • Lyukshina LM, Shishov BH (1988) Biogenic amines in the nervous system of Eudiplozoon nipponicum (Monogenea) (in Russian). In: Sakharov DA (ed) Simple nervous systems. Nauka, Moscow, pp 173–176

  • Mair GR, Maule AG, Shaw C, Johnston CF, Halton DW (1998) Gross anatomy of the muscle systems of Fasciola hepatica as visualized by phalloidin-fluorescence and confocal microscopy. Parasitology 117:75–82

    Article  PubMed  Google Scholar 

  • Marks NJ, Halton DW, Kearn GC, Shaw C, Johnston CF (1994) 5-Hydroxytryptamine-immunoreactivity in the monogenean parasite Entobdella soleae. Int J Parasitol 24:1011–1018

    Article  CAS  PubMed  Google Scholar 

  • Maule AG, Halton DW, Allen JM, Fairweather I (1989) Studies on motility in vitro of the ectoparasitic monogenean, Diclidophora merlangi. Parasitology 98:85–93

    Google Scholar 

  • Maule AG, Halton DW, Johnston CF, Shaw C, Fairweather I (1990a) The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite Diclidophora merlangi. Parasitology 100:255–274

    CAS  PubMed  Google Scholar 

  • Maule AG, Halton DW, Johnston CF, Shaw C, Fairweather I (1990b) A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system of the monogenean parasite Diclidophora merlangi. Parasitol Res 76:409–419

    CAS  PubMed  Google Scholar 

  • McKay DM, Halton DW, Maule AG, Johnston CF, Shaw C, Fairweather I (1991) Putative neurotransmitters in two monogeneans. Helminthologia 28:75–81

    Google Scholar 

  • Prudhoe S (1957) Trematoda. Prac National de l’Upema. I. Mission GF et R Witte en collaboration avec W Adam, A Janssens, L Van Meet et R Verheyen (1946–1949), vol 48, pp 1–28

  • Rahemo ZIF, Gorgees NS (1987) Studies on the nervous system of Polystoma integerrimum as revealed by acetylthiocholine activity. Parasitol Res 73:234–239

    Google Scholar 

  • Reda ES, Arafa SZ (2002) Cholinergic components of the nervous system of the monogenean gill parasites, Pseudodactylogyrus bini and P. anguillae from the eel Anguilla anguilla in Nile Delta waters. Egyptian J Zool 38:41–54

    Google Scholar 

  • Reisinger E (1976) Zur Evolution des stomatogastrischen Nervensystem bei den Platyhelminthen. Z Zool Syst Evolutionsforsch 14:241–252

    Google Scholar 

  • Reuter M (1987) Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system of Gyrodactylus salaris (Monogenea). Acta Zool 68:187–193

    Google Scholar 

  • Reuter M, Mäntylä K, Gustafsson MKS (1998) Organization of the orthogon-main and minor cords. Hydrobiologia 383:175–182

    Article  Google Scholar 

  • Rieger RM, Salvenmoser W, Legneti A, Tyler S (1994) Phalloidin-rhodamine preparations of Macrostomum hystricinum marinum (Platyhelminthes): morphology and postembryonic development of the musculature. Zoomorphology 114:133–147

    Google Scholar 

  • Rohde K (1968) Das Nervensystem der Gattung Polystomoides Ward, 1977 (Monogenea). Z Morphol 62:58–76

    Google Scholar 

  • Rohde K (1972) Fine structure of the Monogenea, especially Polystomoides Ward. Adv Parasitol 10:1–33

    PubMed  Google Scholar 

  • Shaw MK (1982) The fine structure of the brain of Gastrocotyle trachuri (Monogenea: Platyhelminthes) Cell Tissue Res 226:449–460

  • Stewart MT, Mousley A, Koubková B, Šebelová Š, Marks NJ, Halton DW (2002) Gross anatomy of the muscle systems and associated innervation of Apatemon cobitidis proterorhini metacercaria (Trematoda: Strigeidea), as visualised by confocal microscopy. Parasitology 126:273–282

    Article  Google Scholar 

  • Sukhdeo MVK, Hsu SC, Thompson CS, Mettrick DF (1984) Hymenolepis diminuta: behavioural effects of 5-hydroxytryptamine, acetylcholine, histamine and somatostatin. J Parasitol 70:682–688

    CAS  PubMed  Google Scholar 

  • Thompson CS, Mettrick DF (1989) The effects of 5-hydrxyotryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Can J Zool 67:1257–1262

    CAS  Google Scholar 

  • Tinsley RC (1983) Ovoviviparity in platyhelminth life-cycles. Parasitology 86:161–196

    PubMed  Google Scholar 

  • Ward SM, Allen JM, McKerr G (1986) Neuromusculature physiology of Grillotia erinaceus metacestodes (Cestoda: Trypanorhyncha) in vitro. Parasitology 93:587–597

    PubMed  Google Scholar 

  • Zurawski TH, Mousley A, Mair GR, Brennan GP, Maule AG, Gelnar M, Halton DW (2001) Immunomicroscopical observations on the nervous system of adult Eudiplozoon nipponicum (Monogenea: Diplozoidae). Int J Parasitol 31:779–783

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. W. Halton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

El-Naggar, M.M., Arafa, S.Z., El-Abbassy, S.A. et al. Neuromusculature of Macrogyrodactylus clarii, a monogenean gill parasite of the Nile catfish Clarias gariepinus in Egypt. Parasitol Res 94, 163–175 (2004). https://doi.org/10.1007/s00436-004-1198-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-004-1198-1

Keywords

Navigation