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Molecular data show Clinostomoides Dollfus, 1950 is a junior synonym of Clinostomum Leidy, 1856, with redescription of metacercariae of Clinostomum brieni n. comb.

Published online by Cambridge University Press:  14 January 2019

Monica Caffara Open the ORCID record for Monica Caffara [Opens in a new window] ,
Sean A. Locke ,
Ali Halajian ,
Wilmien J. Luus-Powell ,
Deborah Benini ,
Perla Tedesco ,
Gyrhaiss Kapepula Kasembele  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
Ali Halajian
Affiliation:
Department of Biodiversity, University of Limpopo, Private Bag X1106, Sovenga 0727, South Africa
Wilmien J. Luus-Powell
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
Perla Tedesco
Affiliation:
Department of Veterinary Medical Sciences, Alma Mater Studiorum University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia (BO), Italy
Gyrhaiss Kapepula Kasembele
Affiliation:
Unité de recherché en Biodiversité et Exploitation durable des Zones Humides (BEZHU), Faculté des Sciences Agronomiques, Université de Lubumbashi, Haut-Katanga, R.D. Congo
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
*
Author for correspondence: Monica Caffara, E-mail: [email protected]
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Abstract

The genus Clinostomoides Dollfus, 1950 was erected to accommodate a single worm from Ardea goliath sampled in the Belgian Congo. The specimen was distinguished from other clinostomids by its large size and posterior genitalia. In the following years, metacercariae of Clinostomoides brieni, have been described in Clarias spp. in southern and western Africa. A few authors have referred to Clinostomum brieni, but all such usages appear to be lapsus calami, and the validity of Clinostomoides remains widely accepted. In this study our aim was: position C. brieni among the growing clinostomids molecular database, and redescribe the species with emphasis on characters that have emerged as important in recent work. We sequenced two nuclear (partial 18S and ITS) and one mitochondrial marker (partial cytochrome c oxidase I) and studied morphology in metacercariae from hosts and localities likely to harbour the type species (Clarias spp., Democratic Republic of the Congo, South Africa). Phylogenetic analysis shows C. brieni belongs within Clinostomum Leidy, 1856. We therefore transfer C. brieni to Clinostomum, amend the diagnosis for the genus Clinostomum and provide a critical analysis of other species in Clinostomoides, all of which we consider species inquirendae, as they rest on comparisons of different developmental stages.

Keywords

CatfishDNA barcodehalzounheronhybridizationincomplete lineage sortingmolecular prospectingyellow grub
Type
Research Article
Information
Parasitology , Volume 146 , Issue 6 , May 2019 , pp. 805 - 813
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Copyright
Copyright © Cambridge University Press 2019 

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References

Agarwal, SM (1958) Studies on the metacercaria Clinostomoides dollfusi n. sp. (Trematoda: Clinostomatidae) from siluroid fishes. Indian Journal of Helminthology 10, 13–18.Google Scholar
Arthur, JR and Lumanlan-Mayo, S (1997) Checklist of the parasites of fishes of the Philippines. FAO Fisheries Technical Paper, 369, 1–102.Google Scholar
Athokpam, VD, Jyrwa, DB and Tandon, V (2014) Utilizing ribosomal DNA gene marker regions to characterize the metacercariae (Trematoda: Digenea) parasitizing piscine intermediate hosts in Manipur, Northeast India. Journal of Parasitic Diseases 40, 330–338.Google Scholar
Barson, M, Bray, RA, 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.Google Scholar
BirdLife International (2018) IUCN Red List for Birds. Downloaded from http://www.birdlife.org on 5 August 2018.Google Scholar
Briosio-Aguilar, R, García-Varela, M, Hernández-Mena, DI, Rubio-Godoy, M and Pérez-Ponce de León, G (2018) Morphological and molecular characterization of an enigmatic clinostomid trematode (Digenea: Clinostomidae) parasitic as metacercariae in the body cavity of freshwater fishes (Cichlidae) across Middle America. Journal of Helminthology, 1–14. doi: 10.1017/S0022149X18000445.Google Scholar
Caffara, M, Locke, SA, Gustinelli, A, Marcogliese, DJ and Fioravanti, ML (2011) Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. Journal of Parasitology 97, 884–891.Google Scholar
Caffara, M, Locke, SA, Cristanini, C, Davidovich, N, Markovich, MP and Fioravanti, ML (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, SA, Echi, PC, Halajian, A, Benini, D, Luus-Powell, WJ, Tavakol, S and Fioravanti, ML (2017) A morphological and molecular study of Clinostomid metacercariae from African fish with a redescription of Clinostomum tilapiae. Parasitology 144, 1519–1529.Google Scholar
Dollfus, RP (1950) Trématodes récoltés au Congo Belge, par le Professeur Paul Brien. Annales Du Musée Du Congo Belge (Zoologie) 1, 1–136.Google Scholar
Douellou, L (1992). A survey of fish parasites in Lake Kariba, Zimbabwe (1989-1992) final report. University of Zimbabwe, Lake Kariba Research Station ULKRS Bulletin 1/92, 1–72.Google Scholar
Fischthal, JH and Thomas, JD (1970) Some metacercariae of digenetic trematodes in fishes from Nungua Lake, Ghana. Anales del Instituto de Biología Universidad Nacional Autonoma de México Serie Zoología 1, 73–80.Google Scholar
Froese, R and Pauly, D (eds) (2000) FishBase 2000: Concepts, Design and Data Sources. Los Baños, Laguna, Philippines: ICLARM, 344 p.Google Scholar
Gustinelli, A, Caffara, M, Florio, D, Otachi, EO, Wathuta, EM and Fioravanti, ML (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
Hardman, M (2005) The phylogenetic relationships among non-diplomystid catfishes as inferred from mitochondrial cytochrome b sequences; the search for the ictalurid sister taxon (Otophysi: Siluriformes). Molecular Phylogenetics and Evolution 37, 700–720.Google Scholar
Jansen van Rensburg, C, van As, JG and King, PH (2013) New records of digenean parasites of Clarias gariepinus (Pisces: Clariidae) from the Okavango Delta, Botswana, with description of Thaparotrema botswanensis sp. n. (Plathelminthes: Trematoda). African Invertebrates 54, 431–446.Google Scholar
Kanev, I, Radev, V and Fried, B (2002) Family Clinostomidae Lühe, 1901. In Gibson, DI, Jones, A and Bray, R (eds), Keys to the Trematoda, vol. 1. London, UK: CAB International and the Natural History Museum, pp. 113–120.Google Scholar
Kushwaha, B, Kumar, R, Agarwal, S, Pandey, M, Nagpure, NS, Singh, M, Srivastava, S, Joshi, CG, Das, P, Sahoo, L and Jayasankar, P (2015) Assembly and variation analyses of Clarias batrachus mitogenome retrieved from WGS data and its phylogenetic relationship with other catfishes. Meta Gene 5, 105–114.Google Scholar
Lio-Po, G D, Pascual, JP and Santos, JG (1983) Philippines. Paper presented at the Fish quarantine and fish diseases in Southeast Asia. Report of a workshop held in Jakarta, Indonesia, 7–10 December 1982, Jakarta, 35–43.Google Scholar
Locke, SA, Caffara, M, Marcogliese, DJ and Fioravanti, ML (2015) A large-scale molecular survey of Clinostomum (digenea: Clinostomidae). Zoologica Scripta 44, 203–217.Google Scholar
Manter, HW and Pritchard, MH (1969) Some digenetic trematodes of Central Africa chiefly from fishes. Revue de Zoologie et de Botanique Africaines 80, 51–61.Google Scholar
Matthews, D and Cribb, TH (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
Mirzoeva, SS (1981) On the finding of Clinostomoides brieni Dollfus, 1950 (Trematoda: Clinostomatidae) in Azerbaijan. Parazitologiya 15, 288–290 (in Russian).Google Scholar
Mock, DW and Mock, KC (1980) Feeding behavior and ecology of the goliath heron. The Auk 97, 433–448.Google Scholar
Moszczynska, A, Locke, SA, McLaughlin, JD, Marcogliese, DJ and Crease, TJ (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
Pandey, KC (1971) Studies on clinostome metacercaria VIII. On a rare Clinostome metacercaria from Heteropneustes fossilis (Bloch). Proceedings of the Indian Academy of Science 43, 1–3.Google Scholar
Pandey, N (1998) Contribution to our Knowledge of Some Parasites (Monogeneans and Digeneans) of Fishes. PhD thesis Department of Zoology Lucknow University, Lucknow, India. Retrieved from http://ir.amu.ac.in/2333/1/T%205321.pdf (accessed 22 May 2018).Google Scholar
Pandey, KC and Agrawal, N (2013) Metacercarial Fauna of India, Record of Zoological Survey of India. Occasional Paper No. 349: Published by Director, Kolkata: Zoological Survey of India, 1–310..Google Scholar
Pandey, KC and Kiran, (2002) Further observations on Clinostomoides dollfusi Agarwal, 1958. Indian Journal of Helminthology 20, 7–10.Google Scholar
Pandey, KC and Tyagi, V (1986) On a new species of the genus Clinostomoides dollfus, 1950 from Heteropneustes fossilis (Bloch). Indian Journal of Helminthology 3, 83–86.Google Scholar
Pérez-Ponce de León, G, García-Varela, M, Pinacho-Pinacho, CD, Sereno-Uribe, AL and Poulin, R (2016) Species delimitation in trematodes using DNA sequences: middle-American Clinostomum as a case study. Parasitology 143, 1773–1789.Google Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics Evolution 48, 369–371.Google Scholar
Pritchard, MH and Kruse, G (1982) The Collection and Preservation of Animal Parasites. Lincoln, Nebraska: University of Nebraska Press.Google Scholar
Prudhoe, S (1957) Exploration du Parc National de l'Upemba. Mission G. F. de Witte (1946-1949). Trematoda. Institute Parc National Congo Belge, Bruxelles, 48, 1–28.Google Scholar
Rai, P (1970) On the clinostomatid metacercaria in some of our edible fishes and remarks on the pathological significance. Indian Journal of Animal Sciences 40, 189–198.Google Scholar
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Rosser, TG, Baumgartner, WA, Alberson, NR, Noto, TW, Woodyard, ET, King, DT, Wise, DJ and Griffin, MJ (2018) Clinostomum poteae n. sp. (Digenea: Clinostomidae), in the trachea of a double-crested cormorant Phalacrocorax auritus Lesson, 1831 and molecular data linking the lifecycle stages of Clinostomum album Rosser, Alberson, Woodyard, Cunningham, Pote & Griffin, 2017 in Mississippi, USA. Systematic Parasitology 95, 543–566.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, AL, Pinacho-Pinacho, CD, 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
Sereno-Uribe, AL, García-Varela, M, Pinacho-Pinacho, CD and Pérez-Ponce de León, G (2018) Three new species of Clinostomum Leidy, 1856 (Trematoda) from Middle American fish-eating birds. Parasitology Research 117, 2171–2185.Google Scholar
Singh, HS and Sharma, B (1994) Clinostomoides pandeyii n. sp., a rare Clinostome metacercaria from Heteropneustes fossilis (Bloch). Uttar Pradesh Journal of Zoology 14, 91–93.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.Google Scholar
Tubangui, MA and Masiluñgan, VA (1935) Trematode parasites of Philippine vertebrates, VII. Additional records of new species. Philippine Journal of Science 58, 435–446.Google Scholar
Ukoli, FM (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
Woodyard, ET, Rosser, TG and Rush, SA (2017) Alligator wrestling: morphological, molecular, and phylogenetic data on Odhneriotrema incommodum (Leidy, 1856) (Digenea: Clinostomidae) from Alligator mississippiensis Daudin, 1801 in Mississippi, USA. Parasitology Research 116, 2981–2993.Google Scholar
Xia, X and Lemey, P (2009) Assessing substitution saturation with DAMBE. In Lemey, P, Salemi, M and Vandamme, AM (eds), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny, 2nd edn. New York: Cambridge University Press. pp. 615–630.Google Scholar
Xia, X, Xie, Z, Salemi, M, Chen, L and Wang, Y (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.Google Scholar