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A morphological and molecular study of Clinostomid metacercariae from African fish with a redescription of Clinostomum tilapiae

Published online by Cambridge University Press:  27 June 2017

MONICA CAFFARA ,
SEAN A. LOCKE ,
PAUL C. ECHI ,
ALI HALAJIAN ,
DEBORAH BENINI ,
WILMIEN J. LUUS-POWELL ,
SAREH TAVAKOL  and
MARIA L. FIORAVANTI
MONICA CAFFARA*
Affiliation:
Department of Veterinary Medical Sciences, Alma Mater Studiorum University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia, BO, Italy
SEAN A. LOCKE
Affiliation:
Department of Biology, University of Puerto Rico, Box 9000, Mayagüez 00681-9000, Puerto Rico
PAUL C. ECHI
Affiliation:
Department of Zoology and Environmental Biology, Michael Okpara University of Agriculture, Umudike Abia State, Nigeria
ALI HALAJIAN
Affiliation:
Department of Biodiversity, University of Limpopo, Private Bag X1106, Sovenga 0727, South Africa
DEBORAH BENINI
Affiliation:
Department of Veterinary Medical Sciences, Alma Mater Studiorum University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia, BO, Italy
WILMIEN J. LUUS-POWELL
Affiliation:
Department of Biodiversity, University of Limpopo, Private Bag X1106, Sovenga 0727, South Africa
SAREH TAVAKOL
Affiliation:
Department of Biodiversity, University of Limpopo, Private Bag X1106, Sovenga 0727, South Africa
MARIA L. FIORAVANTI
Affiliation:
Department of Veterinary Medical Sciences, Alma Mater Studiorum University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia, BO, Italy
*
*Corresponding author: Department of Veterinary Medical Sciences, Alma Mater Studiorum University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia, BO, Italy. E-mail: monica.caffara@unibo.it
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Summary

The genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) has been reported in all ecozones of the world and a clear separation between the species of the ‘Old World’ and ‘New World’ has been recognized based on molecular studies. Recent works on Afrotropical species include redescriptions of C. cutaneum and C. phalacrocoracis, while C. tilapiae has yet to be studied using modern taxonomic approaches. In the present research, morphological redescription of C. tilapiae metacercariae from a new host, Synodontis batensoda sampled at Anambra River Basin, Nigeria, together with molecular analysis of nuclear internal transcribed spacer rDNA and cytochrome c oxidase 1 mtDNA are reported. We also provide morphological and molecular data from four further putative species of Clinostomum (morphotypes 1–4) from different areas of Africa, as well as the first report of C. phalacrocoracis in South Africa.

Keywords

species delineationcryptic diversityhelminthsparasitesmolecular prospectingfreshwater fishlarvaeDNA barcode
Type
Research Article
Information
Parasitology , Volume 144 , Issue 11 , September 2017 , pp. 1519 - 1529
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Acosta, A. A., Caffara, M., Fioravanti, M. L., Utsunomia, R., Zago, A. C., Franceschini, L. and Josè da Silva, R. (2016). Morphological and molecular characterization of Clinostomum detruncatum (Trematoda: Clinostomidae) metacercaria infecting Synbranchus marmoratus . Journal of Parasitology 102, 151–156.CrossRefGoogle ScholarPubMed
Agbede, S. A., Adeyemo, A. A. and Taiwo, V. O. (2004). Scanning electron microscopic studies of Clinostomum tilapiae Ukoli 1960. Tropical Veterinarian 22, 1–3.CrossRefGoogle Scholar
Aloo, P. A. (2002). A comparative study of helminth parasites from the fish Tilapia zilli and Oreochromis leucostictus in Lake Naivasha and Oloidien Bay, Kenya. Journal of Helminthology 76, 95–102.CrossRefGoogle Scholar
Ayotunde, E. O., Ochang, S. N. and Okey, I. B. (2007). Parasitological examinations and food composition in the gut of feral African carp, Labeo coubie in the Cross River, Southeastern, Nigeria. African Journal of Biotechnology 6, 625–630.Google Scholar
Barson, M., Bray, R., Ollevier, F. and Huyse, T. (2008). Taxonomy and faunistics of the helminth parasites of Clarias gariepinus (Burchell, 1822), and Oreochromis mossambicus (Peters, 1852) from temporary pans and pools in the Save-Runde River floodplain, Zimbabwe. Comparative Parasitology 75, 228–240.CrossRefGoogle Scholar
Batra, V. (1984). Prevalence of helminth parasites in three species of cichlids from a man-made lake in Zambia. Zoological Journal of the Linnean Society 82, 319–333.Google Scholar
Boane, C., Cruz, C. and Saraiva, A. (2008). Metazoan parasites of Cyprinus carpio L. (Cyprinidae) from Mozambique. Aquaculture 284, 59–61.CrossRefGoogle Scholar
Borchsenius, F. (2009). FastGap 1·2. Department of Biosciences, Aarhus University, Denmark. Published online at http://www.aubot.dk/FastGap_home.htm.Google Scholar
Britz, J., Van As, J. G. and Saayman, J. E. (1984). Notes on the morphology of the metacercaria and adult of Clinostomum tilapiae Ukoli, 1966 (Trematoda: Clinostomatidae). South African Wildlife Research 14, 69–72.Google Scholar
Britz, J., Van As, J. G. and Saayman, J. E. (1985). Occurrence and distribution of Clinostomum tilapiae Ukoli, 1966 and Euclinostomum heterostomum (Rudolphi, 1809) metacercarial infections of freshwater fish in Venda and Lebowa, Southern Africa. Journal of Fish Biology 26, 21–28.Google Scholar
Caffara, M., Bruni, G., Paoletti, C., Gustinelli, A. and Fioravanti, M. L. (2014 a). Metacercariae of Clinostomum complanatum (Trematoda: Digenea) in European newts Triturus carnifex and Lissotriton vulgaris (Caudata: Salamandridae). Journal of Helminthology 88, 278–285.Google Scholar
Caffara, M., Davidovich, N., Falk, R., Smirnov, M., Ofek, T., Cummings, D., Gustinelli, A. and Fioravanti, M. L. (2014 b). Redescription of Clinostomum phalacrocoracis metacercariae (Digenea: Clinostomidae) in cichlids from Lake Kinneret, Israel. Parasite 21, 32.CrossRefGoogle ScholarPubMed
Caffara, M., Locke, S. A., Cristanini, C., Davidovich, N., Markovich, M. P. and Fioravanti, M. L. (2016). A combined morphometric and molecular approach to identifying metacercariae of Euclinostomum heterostomum (Digenea: Clinostomidae). Journal of Parasitology 102, 239–248.Google Scholar
Caffara, M., Locke, S. A., Gustinelli, A., Marcogliese, D. J. and Fioravanti, M. L. (2011). Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. Journal of Parasitology 97, 884–891.Google Scholar
Coulibaly, N. D., Salembere, S. and Bessin, R. (1995). Larval Clinostomum infection of cichlid fish in the lake of Kompienga in Burkina Faso: a menace to haleutic exploitation and public health. Cahiers Santé 5, 189–193.Google Scholar
Dollfus, R. P. (1950). Trematodes récoltés au Congo Belge, par le Professeur Paul Brien. Annales Du Musée Du Congo Belge (Zoologie) 1, 1–136.Google Scholar
Dougnon, J., Montchowui, E., Daga, F. D., Houessionon, J., Laleye, P. and Sakiti, N. (2012). Cutaneous and gastrointestinal helminth parasites of the fish Synodontis schall and Synodontis nigrita (Siluriformes: Mochokidae) from the Lower Ouémé Valley in South Benin. Research Journal of Biological Sciences 7, 320–326.Google Scholar
Dubois, G. (1930). Matériaux de la mission scientifique Suisse en Angola. Bulletin de la Société Neuchâteloise des Sciences Naturelles 55, 73–88.Google Scholar
Echi, P. C., Eyo, J. E., Okafor, F. C., Onyishi, G. C. and Ivoke, N. (2012). First record of co-infection of three Clinostomatid parasites in Cichlids (Osteichthyes: Cichlidae) in a tropical freshwater lake. Iranian Journal Public Health 41, 86–90.Google Scholar
Finkelman, S. (1988). Infections of Clinostomatidea in the Sea of Galilee fish. MSc thesis. Faculty of Agriculture, Hebrew University of Jerusalem, Jerusalem.Google Scholar
Fischthal, J. H. and Thomas, J. D. (1970). Some metacercariae of digenetic trematodes in fishes from Nungua Lake, Ghana. Anales del Instituto de Biologia Universidad Nacional Autonoma de Mexico Serie Zoologia 1, 73–80.Google Scholar
Gustinelli, A., Caffara, M., Florio, D., Otachi, E. O., Wathuta, E. M. and Fioravanti, M. L. (2010). First description of the adult stage of Clinostomum cutaneum Paperna, 1964 (Digenea: Clinostomidae) from grey herons Ardea cinerea L. and a redescription of the metacercaria from the Nile tilapia Oreochromis niloticus niloticus (L.) in Kenya. Systematic Parasitology 76, 39–51.Google Scholar
Jansen van Rensburg, C., van As, J. G. and King, P. H. (2003). Clinostomum species infecting the sharptooth catfish, Clarias gariepinus in the Okavango Delta, Botswana. Parasitological Society of Southern Africa 74, 87–101.Google Scholar
Kabunda, M. Y. and Sommerville, C. (1984). Parasitic worms causing the rejection of tilapia (Oreochromis species) in Zaire. The British Veterinary Journal 140, 263–268.CrossRefGoogle ScholarPubMed
Katoh, K., Misawa, K., Kuma, K. I. and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.CrossRefGoogle ScholarPubMed
Khalil, L. F. and Thurston, J. P. (1973). Studies on the helminth parasites of freshwater fishes of Uganda including the descriptions of two new species of digeneans. Revue de Zoologie et de Botanique Africaines 87, 209–248.Google Scholar
Locke, S. A., Al-Nasiri, F. S., Caffara, M., Drago, F., Kalbe, M., Lapierre, A. R., McLaughlin, J. D., Nie, P., Overstreet, R. M., Souza, G. T. and Takemoto, R. M. (2015 a). Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal for Parasitology 45, 841–855.Google Scholar
Locke, S. A., Caffara, M., Marcogliese, D. J. and Fioravanti, M. L. (2015 b). A large-scale molecular survey of Clinostomum (Digenea: Clinostomidae). Zoologica Scripta 44, 203–217.CrossRefGoogle Scholar
Lombard, G. L. (1968). A survey of fish diseases and parasites encountered in Transvaal. Limnological Society of Southern Africa Newsletter 11, 23–29.Google Scholar
Luus-Powell, W. J., Molele, R. A., Tavakol, S., Matla, M. M., Halajian, A. and Fouché, P. S. O. (2015). The parasite diversity of Amphilius uranoscopus and Chiloglanis pretoriae in the Vhembe biosphere reserve, Limpopo province, South Africa. In 9th International Symposium on Fish Parasites, Valencia, Spain, 31 August–4 September 2015, p. 164.Google Scholar
Madanire-Moyo, G. N., Luus-Powell, W. J. and Olivier, P. A. (2012). Diversity of metazoan parasites of the Mozambique tilapia, Oreochromis mossambicus (Peters, 1852), as indicators of pollution in the Limpopo and Olifants River systems. Onderstepoort Journal of Veterinary Research 79, 1–9.Google Scholar
Manter, H. W. and Pritchard, M. H. (1969). Some digenetic trematodes of Central Africa chiefly from fishes. Revue de Zoologie et de Botanique Africaines 80, 51–61.Google Scholar
Marwan, A. and Mohammed, T. A. (2003). Scanning electron microscopy of Clinostomum metacercaria from Oreochromis niloticus from Assiut, Egypt. Egyptian Journal of Biology 5, 70–77.Google Scholar
Matthews, D. and Cribb, T. H. (1998). Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni from Egretta intermedia . Systematic Parasitology 39, 199–208.Google Scholar
Moszczynska, A., Locke, S. A., McLaughlin, J. D., Marcogliese, D. J. and Crease, T. J. (2009). Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 75–82.Google Scholar
Nolan, M. J. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 101–163.CrossRefGoogle ScholarPubMed
Ochieng, V. O., Matolla, G. K. and Khyria, S. K. (2012). A study of Clinostomum affecting Oreochromis niloticus in small water bodies in Eldoret-Kenya. International Journal of Scientific & Engineering Research 3, 1–6.Google Scholar
Okaka, C. E. and Akhigbe, J. E. (1999). Helminth parasites of some tropical freshwater fish from Osse River in Benin, southern Nigeria. Tropical Freshwater Biology 8, 41–48.Google Scholar
Okoye, I. C., Abu, S. J., Obiezue, N. N. R. and Ofoezie, I. E. (2014). Prevalence and seasonality of parasites of fish in Agulu Lake, Southeast, Nigeria. African Journal of Biotechnology 13, 502–508.Google Scholar
Olurin, K., Okafor, J., Alade, A., Asiru, R., Ademiluwa, R., Owonifari, K. and Oronay, O. (2012). Helminth parasites of Sarotherodon galilaeus and Tilapia zilli (Pisces: Cichlidae) from River Oshun, Southwest Nigeria. International Journal of Aquatic Science 3, 49–55.Google Scholar
Olurin, K. B. and Somorin, C. A. (2006). Intestinal helminths of the fishes of Owa Stream, South-west Nigeria. Research Journal of Fisheries and Hydrobiology 1, 6–9.Google Scholar
Onyedineke, N. E., Obi, U., Ofoegbu, P. U. and Ukogo, I. (2010). Helminth parasites of some freshwater fish from River Niger at Illushi, Edo state, Nigeria. Journal of American Science 6, 16–21.Google Scholar
Ortlepp, R. J. (1935). On the metacercaria and adult of Clinostomum van der horsti sp. n. a trematode parasite of fish and herons. Onderstepoort Journal of Veterinary Science and Animal Industry 5, 51–58.Google Scholar
Paperna, I. (1980). Parasites, Infections and Diseases of Fish in Africa, Vol. 7. CIFA Technical Papers, FAO, Roma.Google Scholar
Pérez-Ponce de León, G., García-Varela, M., Pinacho-Pinacho, C. D., Sereno-Uribe, A. L. and Poulin, R. (2016). Species delimitation in trematodes using DNA sequences: middle-American Clinostomum as a case study. Parasitology 143, 1773–1789.CrossRefGoogle ScholarPubMed
Pinto, H. A., Caffara, M., Fioravanti, M. L. and Melo, A. L. (2015). Experimental and molecular study of cercariae of Clinostomum sp. (Trematoda: Clinostomidae) from Biomphalaria spp. (Mollusca: Planorbidae) in Brazil. Journal of Parasitology 101, 108–113.Google Scholar
Pritchard, M. H. and Kruse, G. (1982). The Collection and Preservation of Animal Parasites. University of Nebraska Press, Lincoln, Nebraska.Google Scholar
Ramollo, P. P., Luus-Powell, W. J. and Jooste, A. (2006). Impact of water quality on abundance of parasites from Oreochromis mossambicus at the Phalaborwa Industrial Complex (PIC) and Barrage: preliminary results. Parasitological Society of Southern Africa 77, 92–103.Google Scholar
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3·2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Rosser, T. G., Alberson, N. R., Woodyard, E. T., Cunningham, F. L., Pote, L. M. and Griffin, M. J. (2017). Clinostomum album n. sp. and Clinostomum marginatum (Rudolphi, 1819), parasites of the great egret Ardea alba L. from Mississippi, USA. Systematic Parasitology 94, 35–49.Google Scholar
Senapin, S., Phiwsaiya, K., Laosinchai, P., Kowasupat, C., Ruenwongsa, P. and Panijpan, B. (2014). Phylogenetic analysis of parasitic trematodes of the genus Euclinostomum found in Trichopsis and Betta fish. Journal of Parasitology 100, 368–371.Google Scholar
Sereno-Uribe, A. L., Pinacho-Pinacho, C. D., García-Varela, M. and Pérez-Ponce de León, G. (2013). Using mitochondrial and ribosomal DNA sequences to test the taxonomic validity of Clinostomum complanatum Rudolphi, 1814 in fish-eating birds and freshwater fishes in Mexico, with the description of a new species. Parasitology Research 112, 2855–2870.Google Scholar
Smit, W. J. and Luus-Powell, W. J. (2012). The occurrence of metazoan endoparasites of Schilbe intermedius Rüppell, 1832 from the Nwanedi-Luphephe Dams in the Limpopo River System, South Africa. African Zoology 47, 35–41.Google Scholar
Taher, G. A. (2009). Some studies on metacercarial infection in Oreochromis niloticus in Assiut governorate and their role in transmission of some trematodes to dogs. Assiut University Bulletin for Environmental Researches 12, 63–79.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Ukoli, F. M. (1966). On Clinostomum tilapiae n. sp., and C. phalacrocoracis Dubois, 1931 from Ghana, and a discussion of the systematics of the genus Clinostomum Leidy, 1856. Journal of Helminthology 40, 187–214.Google Scholar
Williams, M. O. and Chaytor, D. E. B. (1966). Some helminth parasites of fresh water fishes of the Freetown peninsula, Sierra Leone. Bulletin de l'Institut Fondamental d'Afrique Noire. Série A: Sciences Naturelles 28, 563–575.Google Scholar
Yimer, E. (2000). Preliminary survey of parasites and bacterial pathogens of fish at Lake Ziway. Ethiopian Journal of Science 23, 25–33.Google Scholar
Yimer, E. and Enyew, M. (2003). Parasites of fish at Lake Tana, Ethiopia. Ethiopian Journal of Science 26, 31–36.Google Scholar
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