Skip to main content
Log in

Histopathological and ultrastructural studies of a Henneguya species (Myxozoa: Myxosporea) infesting the intestine of Clarias gariepinus from Benin (West Africa)

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

Abstract

Fish culture is the best alternative to fill the gap between natural fish catches and estimated needs of populations in animal protein consumption. In West Africa, this goal required to have suitable fishes for aquaculture which are Clariidae and Tilapia. Clarias gariepinus (Clariidae) fetches a higher price than tilapias as it can be sold alive at the market but a high infestation by Henneguya leads to decrease this commercial value. Those reasons lead us to perform studies on seasonal variations, histopathological aspects and life cycle of Henneguya sp. infecting the intestine of C. gariepinus using light and electron microscope. From November 2011 to December 2012, 339 specimens were collected from Ouémé River (Benin) and examined. An overall prevalence of 7.37 % was recorded for plasmodia of Henneguya sp. Parasite occurrence did not vary significantly between seasons (χ2 = 12.235; df = 3; p > 0.05), nor sexes (χ2 = 2.992; df = 7; p > 0.05) while differences were significant between classes of weight (χ2 = 39.929; df = 5; p < 0.05). The highest prevalence was recorded in host ranging from 300 to 374 g. Histopathological analysis showed that the mass continuous development of the plasmodium produced thickening of the intestine wall and compressed neighboring tissues and destroyed villi and smooth muscle layers. The stages of the parasite development including sporogenesis, capsulogenesis, and valvogenesis were asynchronous. Investigations are still running by molecular approaches in order to identify accurately this species.

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. 2
Fig. 3
Figs. 4–12
Figs. 13–19
Figs. 20–23

Similar content being viewed by others

References

  • Abdel-Ghaffar F, Abdel-Aziz A, Ezz El-Din N, Naas S (1995) Light and electron microscopic studies on Henneguya branchialis (Ashmawy et al. 1989) (Myxosporea: Myxozoa) infecting the catfish Clarias gariepinus in the River Nile Egypt. J Union Arab Biol 3(A):113–133

    Google Scholar 

  • Abdel-Ghaffar F, Ibrahim EA, Bashtar A, Ali MA (1998) Myxosporidia infecting saline and freshwater fishes of Qarun and Wadi El-Raiyan lakes, Egypt. J Egypt Ger Soc Zool (D) 26:209–229

    Google Scholar 

  • Abdel-Ghaffar F, Abdel-Baki AS, Bayoumy E, Bashtar AR, Al-Quraishy S, Morsy KS, Alghamdy A, Mehlhorn H (2008) Light and electron microscopic study on Henneguya suprabranchiae Landsberg, 1987 (Myxozoa: Myxosporea) infecting Oreochromis niloticus, a new host record. Parasitol Res 103:609–617

    Article  PubMed  Google Scholar 

  • Adriano EA, Arana S, Cordeiro NS (2005) Histology, ultrastructure and prevalence of Henneguya plaractus (Myxosporea) infecting the gills of Plaractus mesopotamicus (Characidae) cultivated in Brazil. Dis Aquat Org 64:229–235

    Article  PubMed  CAS  Google Scholar 

  • Adriano EA, Arana S, Alves AL, Silva MRM, Ceccarelli PS, Henrique-Silva F, Maia AAM (2009) Myxobolus cordeiroi n. sp., a parasite of Zungaro jahu (Siluriformes: Pimelodiade) from Brazilian Pantanal: morphology, phylogeny and histopathology. Vet Parasitol 162:221–229

    Article  PubMed  CAS  Google Scholar 

  • Ali MA (1999) Henneguya ghaffari sp. n. (Myxozoa: Myxosporea) infecting the Nile perch Lates niloticus (Teleostei: Centropomidae). Dis Aquat Org 38:225–230

    Article  PubMed  CAS  Google Scholar 

  • Ali MA, Al-Rasheid AS, Sakran T, Abdel-baki AS, Abdel-Ghaffar FA (2002) Some species of the genus Myxobolus (Myxozoa: Myxosporea) infecting freshwater fishes of the River Nile, Egypt. Parasitol Res 88:9–15

    PubMed  Google Scholar 

  • Ali MA, Abdel-Baki AS, Sakran T, Entzeroth R, Abdel-Ghaffar F (2007) Myxobolus lubati n. sp. (Myxosporea: Myxobolidae), a new parasite of haffara seabream Rhabdosargus haffara (Forsskal, 1775), Red Sea, Egypt: a light and transmission electron microscopy. Parasitol Res 100:819–827

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Pellitero P, Palenzuela O, Sitja-Bobadilla A (2008) Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol Int 57:110–120

    Article  PubMed  CAS  Google Scholar 

  • Anon (Anonymous): Direction des pêches (2011) Rapport Annuel d’Activité. Ministère de l’Agriculture, de l’Elevage et de la Pêche, République du Bénin. 72p

  • Azevedo C, Matos E (1989) Some ultrastructural data on the spore development in a Henneguya sp. parasite of the gill of a Brazilian fish. Parasitol Res 76:131–134

    Article  PubMed  CAS  Google Scholar 

  • Azevedo C, Lom J, Corral L (1989) Ultrastructural aspects of Myxidium giardi (Myxozoa: Myxosporea) parasite of the European eel Anguilla anguilla. Dis Aquat Org 6:55–61

  • Bahri S (2008) Abnormal forms of Myxobolus bizerti and Myxobolus mülleri (Myxosporea: Bivalvulida) spores with caudal appendages. Bull Eur Assoc Fish Pathol 20:252–255

    Google Scholar 

  • Barassa B, Adriano EA, Cordeiro NS, Arana S, Ceccarelli PS (2012) Morphology and host–parasite interaction of Henneguya azevedoi n. sp., parasite of gills of Leporinus obtusidens from Mogi-Guaçu River, Brazil. Parasitol Res 110:887–894

    Article  PubMed  Google Scholar 

  • Carriero MM, Adriano EA, Silva MRM, Ceccarelli PS, Maia AM (2013) Molecular phylogeny of Myxobolus and Henneguya genera with several New South America species. Plos ONE 8:e73713

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Current WL, Janovy J Jr (1976) Ultrastructure of interlamellar Henneguya exilis in the channel catfish. J Parasitol 62:975–998

    Article  PubMed  CAS  Google Scholar 

  • Current WL, Janovy J Jr (1977) Sporogenesis in Henneguya exilis infecting the Channel catfish: an ultrastructural study. Protistologica 13:157–167

    Google Scholar 

  • Current WL, Janovy J Jr (1978) Comparative study of ultrastructure of interlamellar and intralamellar types of Henneguya exilis Kudo from channel catfish. J Protozool 25:56–65

    Article  PubMed  CAS  Google Scholar 

  • Current WL, Janovy J Jr, Knight SA (1979) Myxosoma funduli Kudo (Myxosporida) in Fundulus kansae : ultrastructure of the plasmodium wall and sporogenesis. J Protozool 26:574–583

    Article  Google Scholar 

  • Desser SS, Paterson WB (1978) Ultrastructural and cytochemical observation on sporogenesis of Myxobolus sp. (Myxosporidia) from common shiner Natropis coronutus. J Protozool 25:314–326

    Article  PubMed  CAS  Google Scholar 

  • Desser SS, Molnar K, Weiller I (1983) Ultrastructure of sporogenesis of Thelohanellus nikolskii Akkhmerov, 1955 (Myxozoa: Myxosporea) from the common carp Cyprinus carpio. J Parasitol 69:504–518

    Article  Google Scholar 

  • Eiras JC (2002) Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 52:43–54

    Article  PubMed  CAS  Google Scholar 

  • Eiras JC, Adriano EA (2012) A checklist of new species of Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae) described between 2002 and 2012. Syst Parasitol 83:95–104

    Article  PubMed  CAS  Google Scholar 

  • El-Mansy A, Bashtar AR (2002) Histopathological and ultrastructural studies of Henneguya suprabranchiae Landsberg, 1987 (Myxosporea: Myxobolidae) parasitizing the suprabranchial organ. Parasitol Res 88:617–626

    Article  PubMed  CAS  Google Scholar 

  • El-Matbouli M, Hoffmann RW (1989) Experimental transmission of two Myxobolus spp developing bisporogony via tubificid worms. Parasitol Res 75:461–464

    Article  PubMed  CAS  Google Scholar 

  • El-Matbouli M, Fischer-Scherl T, Hoffmann RW (1990) Light and electron microscopic studies on Myxobolus cotti El-Matbouli and Hoffmann, 1987 infecting the central nervous system of the bullhead (Cottus gobio). Parasitol Res 76:219–227

    Article  PubMed  CAS  Google Scholar 

  • Ernst II, Whttingtton D, Corneillte S, Talbot C (2005) Effects of temperature, salinity, desiccation and chemical treatments on egg embryonation and hatching success of Benedenia seriolae (Monogenea: Capsalidae), a parasite of farmed Seriola spp. J Fish Dis 28:157–164

  • Estensoro I, Redondo JM, Alvarez-Pellitero P, Sitja-Bobadilla A (2010) Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata. Dis Aquat Org 92:51–58

    Article  PubMed  Google Scholar 

  • Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exhange, osmoregulation, acid–base regulation and excretion of nitrogenous waste. Physiol Revs 85:97–177

    Article  CAS  Google Scholar 

  • FAO (2012) La situation mondiale des pêches et de l’aquaculture 2012, Rome, 241p

  • Feist SW, Longshaw M (2005) Myxozoan diseases of fish and effects on host populations. Acta Zool 51:758–760

    Google Scholar 

  • Feist SW, Longshaw M (2006) Phylum myxozoa. In Woo PTK editor. Fish diseases and disorders. Protozoan and metazoan infections. Vol. 1, 2nd ed. CAB International, Oxfordshire, pp 230–296

    Book  Google Scholar 

  • Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534

    Article  PubMed  CAS  Google Scholar 

  • Gbankoto A, Pampoulie C, Marques A, Sakiti GN (2001a) Occurrence of myxosporean parasites in the gills of two tilapia species from Lake Nokoué (Benin, West Africa): effect of host size and sex, and seasonal patterns of infection. Dis Aquat Org 44:217–222

    Article  PubMed  CAS  Google Scholar 

  • Gbankoto A, Pampoulie C, Marques A, Sakiti GN (2001b) Myxobolus dahomeyensis infection in ovaries of tilapia species from Bénin (West Africa). J Fish Biol 58:883–886

    Article  Google Scholar 

  • Gbankoto A, Pampoulie C, Marques A, Sakiti GN, Dramane KL (2003) Infection patterns of Myxobolus heterospora in two tilapia species (Teleostei: Cichlidae) and its potential effects. Dis Aquat Org 55:125–131

    Article  PubMed  CAS  Google Scholar 

  • Ghaffar FA, El-Shahawi G, Naas S (1995) Myxosporidia infecting some Nile fishes in Egypt. Parasitol Res 81:163–166

    Article  PubMed  Google Scholar 

  • Haaparanta A, Valtonen ET, Hoffman RW (1994) Pathogenicity and seasonal occurrence of Hennuguya creplini (Protozoa, Myxosporea) on the gills of perch Perca fluviatilis in central Finland. Dis Aquat Org 20:15–22

    Article  Google Scholar 

  • Hwang PP, Lee TH (2007) News insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A 148:479–497

    Article  CAS  Google Scholar 

  • Iwanowicz DD, Iwanowicz LR, Howerth EW, Schill WB, Blazer VS, Johnson RL (2013) Characterization of a new myxozoan species (Myxozoa: Myxobolidae: Myxosporea) in large scale stonerollers (Campostoma oligolepis) from the mobile river basin (Alabama). J Parasitol 99:102–111

    Article  PubMed  CAS  Google Scholar 

  • Karasov WH, Hume ID (1997) Vertebrate gastrointestinal system. In: Dantzler WH (ed) In the handbook of physiology: comparative physiology, vol. 1. Oxford University Press, Oxford, pp 409–480

    Google Scholar 

  • Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffman RW, Khattra J, Halllett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48(4):395–413

    Article  PubMed  CAS  Google Scholar 

  • Khidr AA, Said AE, Samak OAA, Sheref SEA (2012) The impacts of ecological factors on prevalence, mean intensity and seasonal changes of the monogenean gill parasite, Microcotyloides sp., infesting the Terapon puta fish inhabiting coastal region of Mediterranean Sea at Damietta region. J Basic & Appl Zool 65:109–115

  • Landsberg JH (1985) Myxosporean infections in cultured tilapias in Israel. J Protozool 32:194–201

    Article  PubMed  CAS  Google Scholar 

  • Lazard J, Legendre M (1994) La pisciculture africaine: enjeux et problèmes de recherche. Cah Agri 3:83–92

    Google Scholar 

  • Li Y, Sato H, Kamata Y, Ohnishi T, Sugita-Konishi Y (2012) Three novel myxobolid species of genera Henneguya and Myxobolus (Myxosporea: Bivalvuvulida) from marine fish in Japan. Parasitol Res 111:819–826

    Article  PubMed  Google Scholar 

  • Liu Y, Gu ZM, Luo LY (2010) Some additional data to the occurrence, morphology and validity of Myxobolus turpisrotundus Zhang, 2009 (Myxozoa: Myxosporea). Parasitol Res 107:67–73

    Article  PubMed  CAS  Google Scholar 

  • Lodish H, Berk A, Matsudaira P, Kaiser CA, Krieger M, Scott MP, Zipursky L, Darnell J (2005) Biologie Moléculaire de la Cellule, Ed. de boeck, Espagne. 973p

  • Lom J, Arthur JR (1989) A guideline for the preparation of species description in Myxosporea. J Fish Dis 12:151–156

    Article  Google Scholar 

  • Lom J, de Puytorac P (1965) Studies on the myxosporidian ultrastructure and polar capsule development. Protistol 1:53–65

    Google Scholar 

  • Lom J, Dykova I (1992a) Protozoan parasites of fishes. Developments in Aquaculture and Fisheries Science Vol.26, Elsevier, 315p

  • Lom J, Dykova I (1992b) Fine-structure of triactinomyxon early stages and sporogony myxosporean and actinosporean features compared. J Protozool 39:16–27

    Article  Google Scholar 

  • Lom J, Dykova I (1994) Studies on protozoan parasites of Australian fishes III. Species of genus Myxobolus Bütschli, 1882. Eur J Protistol 30:431–439

    Article  Google Scholar 

  • Lom J, Dykovà I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36

    Article  PubMed  Google Scholar 

  • Lom J, Noble ER (1984) Revised classification of the class Myxosporea Butschli, 1881. Folia Parasitol (Praha) 31:193–205

    Google Scholar 

  • Lom J, Feist SW, Dykova I, Kepr T (1989) Brain myxoboliasis of bullhead, Cottus gobio L., due to Myxobolus jiroveci sp. n.: light and electron microscope observations. J Fish Dis 12:15–27

    Article  Google Scholar 

  • Lom J, Rohde K, Dykova I (1992) Studies on protozoan parasites of Australian fishes I. New species of the genera Coccomyxa Léger et Hess, 1907, Ortholinea Shulman, 1962 and Kudoa Meglitsch, 1947 (Myxozoa, Myxosporea). Folia Parasitol 39:289–306

    Google Scholar 

  • Matos E, Tajdari J, Azevedo C (2005) Ultrastructural studies of Henneguya rhamdia n. sp. (Myxozoa) a parasite from the Amazon teleost fish, Rhamdia quelen (Pimelodidae). J Eukaryot Microbiol 52(6):532–537

    Article  PubMed  Google Scholar 

  • McCraren JP, Landolt ML, Hoffman GL, Meyer FP (1975) Variation in response of channel catfish to Henneguya sp infections (Protozoa: Myxosporidia). J Wildl Dis 11:2–7

    Article  Google Scholar 

  • Milanin T, Eiras JC, Arana S, Maia AAM, Alves AL, Silva MRM, Carriero MM, Ceccarelli PS, Adriano EA (2010) Phylogeny, ultrastructure, histopathology and prevalence of Myxobolus oliveirai sp. nov., a parasite of Brycon hilarii (Characidae) in the Pantanal wetland, Brazil. Mem Inst Oswaldo Cruz 105:762–769

    Article  PubMed  Google Scholar 

  • Molnár K (1979) Myxobolus pavlovskii (Achmerov, 1954) (Myxosporidia) infection in the silver carp and bighead. Acta Vet Hung 3:207–2l6

    Google Scholar 

  • Molnár K, Eszterbauer E, Székely C, Dán A, Harrach B (2002) Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. J Fish Dis 25:643–652

    Article  Google Scholar 

  • Morsy K, Abdel-Ghaffar F, Bashtar A-R, Mehlhorn H, Al Quraishy S, Abdel-Gaber R (2012) Morphology and small subunit ribosomal DNA sequence of Henneguya suprabranchiae (Myxozoa), a parasite of the catfish Clarias gariepinus (Clariidae) from the River Nile, Egypt. Parasitol Res 111:1423–1435

    Article  PubMed  Google Scholar 

  • Munoz P, Sitja-Bobadilla A, Alvarez-Pellitero P (2000) Antigenic characterization of Sphaerospora dicentrarchi (Myxospora: Bivalvulida), a parasite from European seabass Dicentrarchus labrax (Teleostei: Serranidae). Dis Aquat Org 40:117–124

    Article  PubMed  CAS  Google Scholar 

  • Muzzall PM (1995) Distribution of Myxobolus scleroperca (Myxobolidae: Myxosporea) in yellow perch (Perca flavescens) in the Great Lakes. J Parasitol 81:498–499

    Article  PubMed  CAS  Google Scholar 

  • Obiekezie AI, Enyenihi MK (1988) Henneguya chrysichthyi sp, nov. (Protozoa: Myxozoa) from the gills of estuarine catfish Chrysichthys nigrodigitatus (Lacepède) (Pisces: Bagridae) in Nigeria. J. Afr Zool 102:33–42

    Google Scholar 

  • Okaeme AN, Obiekeziz AI, Lehman J, Antai EE, Madu CT (1988) Parasites and diseases of cultured fish of Lake Kainji area Nigeria. J Fish Biol 32:479–481

    Article  Google Scholar 

  • Palenzuela O (2006) Myxozoan infections in Mediterranean mariculture. Parasitologia 48:27–29

    CAS  Google Scholar 

  • Pulsford A, Matthews RA (1982) An ultrastructure study of Myxobolus exiguus Thelohan, 1895 (Myxosporea) from gray mullet, Crenimugil labrosus (Risso). J Fish Dis 5:509–526

    Article  Google Scholar 

  • Rigos G, Katharios P (2010) Pathological obstacles of newly-introduced fish species in Mediterranean mariculture: a review. Rev Fish Biol Fish 20:47–70

    Article  Google Scholar 

  • Sakiti GN, Blanc E, Marques A, Bouix G (1991) Myxosporidies (Myxozoa : Myxosporea) du genre Myxobolus Bütschli, 1882, parasites de poissons Cichlidae du Lac Nokoué au Bénin (Afrique de l’Ouest). J Afr Zool 105:173–186

    Google Scholar 

  • Sakiti GN, Tarer V, Jacquemin D, Marques A (1996) Présence en Méditerranée occidentale d’une Myxosporidie histozoïque pathogène dans les élevages de daurade, Sparus aurata L. Ann Sci Nat B 17:123–127

    Google Scholar 

  • Sakiti N, Kabré G, Marques A, Dossou C (1999) Gill diseases caused by Myxozoa in fishes of Inland waters of the south of Benin. J Eukaryot Microbiol 46:15A

    Google Scholar 

  • Schmahl G, Mehlhorn H, Taraschewski H (1989) Treatment of fish parasites. 5. The effects of sym. Triazinone (Toltrazuril) on skin parasitic Ciliophora (Ichthyophthirius multifilis Fouquet, 1876, Glossatella amoebae Grenfell, 1884, and Trichodina sp. Ehrenberg, 1831). Eur J Protistol 24:152–161

    Article  PubMed  CAS  Google Scholar 

  • Stehr C (1986) Sporogenesis of the myxosporean Kudoa paniformis Kabata & Whitaker, 1981 and Kudoa thyrsites (Gilchrist, 1924) in the muscle of Pacific whiting, Merluccius productus (Ayres): an ultrastructural study. J Fish Dis 9:505–517

    Article  Google Scholar 

  • Swanson C (1998) Interactive effects of metabolic rate, activity, growth and osmoregulation in the euryhaline milkfish (Chanos chanos). J Exp Biol 201:3355–3366

    PubMed  Google Scholar 

  • Tossavi ND, Gbankoto A, Adite A, Ibikounle M, Grunau C, Sakiti GN (2014) Metazoan parasite communities of Catfishes (Teleostei: Siluridae) in Benin: West Africa. Parasitol Res 113:3973–3983

    Article  PubMed  Google Scholar 

  • Tseng YC, Hwang PP (2008) Some insights into metabolism for osmoregulation in fish. Comp Biochem Physiol C 148:419–429

    Google Scholar 

  • Viozzi GP, Flores VR (2003) Myxidium biliare sp. n. (Myxozoa) from gall bladder of Galaxias maculates (Osmeriformes: Galaxiidae) in Patagonia (Argentina). Folia Parasitol 50:190–194

    Article  PubMed  Google Scholar 

  • Von Heijne G (1999) Recent advances in the understanding of membrane protein assembly and structure. Q Rev Biophys 32:285–307

    Article  Google Scholar 

  • Wieser W, Medgyesy N (1991) Metabolic rate and cost of growth in juvenile pike (Esox lucius L.) and fresh perch (Perca fluviatilis L.): the use of energy budgets as indicators of environmental change. Ecologica 87:500–505

    Google Scholar 

  • Zhang JY, Al-Quraishy S, Abdel-Baki AS (2014) The morphological and molecular characterization of Myxobolus khaliji n. sp. (Myxozoa: Myxosporea) from the double bar sea bream Acanthopagrus bifasciatus (Forsskål, 1775) in the Arabian Gulf, Saudi Arabia. Parasitol Res 113:2177–2183

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

NDT is thankful to Prof Thierry NOGUER, headmaster of the Institut de Modélisation et d’Analyse en Géo-Environnement et Santé (IMAGES) of UPVD, for taking a great interest in his work and for providing laboratory facilities during his stay at Perpignan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nounagnon Darius Tossavi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tossavi, N.D., Gbankoto, A., Yessoufou, A. et al. Histopathological and ultrastructural studies of a Henneguya species (Myxozoa: Myxosporea) infesting the intestine of Clarias gariepinus from Benin (West Africa). Parasitol Res 114, 861–872 (2015). https://doi.org/10.1007/s00436-014-4249-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4249-2

Keywords

Navigation