Abstract
In the Afrotropic region, the genus Clinostomum is represented by four accepted and four unnamed species distinguished using molecular data. Here, we describe one of the four unnamed species as Clinostomum ukolii n. sp. based on metacercariae from siluriform fishes (Synodontis batensoda, Schilbe intermedius) collected in Nigeria and South Africa. The new species is distinguished by molecular data (39 new sequences of partial cytochrome c oxidase I ≥ 6.7% divergent from those of other species) and morphological differences from named and unnamed species in the same region. Metacercariae of C. ukolii n. sp. can be distinguished based on size, tegumental spines, and various aspects of the genital complex, including its position, lobation of the anterior testis, and the disposition and shape of the cirrus pouch. Although descriptions of new species of digeneans are typically based on the morphology of adults, we argue that in cases where data are available from metacercariae from regionally known species, new species can be described based on metacercariae, particularly when supported by molecular data, as here. Moreover, sub-adult reproductive structures can be clearly visualized in metacercaria of Clinostomum. Considering metacercariae as potential types for new species could advance clinostome systematics more rapidly, because metacercariae are encountered much more often than adults in avian definitive hosts.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aboel Hadid SM, Lotfy HS (2007) Some studies on helminth parasites of buff backed heron (Ardeola ibis ibis) with special reference to its role in transmission of Clinostomum complanatum in Beni-Suef Governorate. Beni-Suef Vet Med J:135–141
Acosta AA, Caffara M, Fioravanti ML, Utsunomia R, Zago AC, Franceschini L, José da Silva R (2016) Morphological and molecular characterization of Clinostomum detruncatum (Trematoda: Clinostomidae) metacercaria infecting Synbranchus marmoratus. J Parasitol 102:151–156. https://doi.org/10.1645/15-773
Barson M, Bray R, Ollevier F, 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. Comp Parasitol 75:228–240. https://doi.org/10.1654/4337.1
Batra V (1984) Prevalence of helminth parasites in three species of cichlids from a man-made lake in Zambia. Zool J Linnean Soc 82:319–333. https://doi.org/10.1111/j.1096-3642.1984.tb00646.x
Briosio-Aguilar R, Pinto HA, Rodríguez-Santiago MA, López-García K, García-Varela M, Pérez-Ponce de León G (2018) Link between the adult and the metacercaria of Clinostomum heluans Braun, 1899 (Trematoda: Clinostomidae) through DNA sequences, and its phylogenetic position within the genus Clinostomum Leidy, 1856. J Parasitol 104:292–296. https://doi.org/10.1645/17-183
Caffara M, Locke SA, Gustinelli A, Marcogliese DJ, Fioravanti ML (2011) Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. J Parasitol 97:884–891. https://doi.org/10.1645/GE-2781.1
Caffara M, Davidovich N, Falk R, Smirnov M, Ofek T, Cummings D, Gustinelli A, Fioravanti ML (2014) Redescription of Clinostomum phalacrocoracis metacercariae (Digenea: Clinostomidae) in cichlids from Lake Kinneret, Israel. Parasite 21:32. https://doi.org/10.1051/parasite/2014034
Caffara M, Locke SA, Echi PC, Halajian A, Benini D, Luus-Powell WJ, Tavakol S, Fioravanti ML (2017) A morphological and molecular study of Clinostomid metacercariae from African fish with a redescription of Clinostomum tilapiae. Parasitology 144:1519–1529. https://doi.org/10.1017/S0031182017001068
Caffara M, Locke SA, Halajian A, Luus-Powell WJ, Benini D, Tedesco P, Kapepula Kasembele G, Fioravanti ML (2019) Molecular data show Clinostomoides Dollfus, 1950 is a junior synonym of Clinostomum Leidy, 1856, with redescription of metacercariae of Clinostomum brieni n comb. Parasitology 146:805–813. https://doi.org/10.1017/S0031182018002172
Dubois G (1930) Materiaux de la mission scientifique Suisse en Angola. Bull Soc Neuchl Sci Nat 55:73–88
Echi PC, Eyo JE, Okafor FC, Onyishi GC, Ivoke N (2012) First record of co-infection of three clinostomatid parasites in cichlids (Osteichthyes: Cichlidae) in a tropical freshwater lake. Iran J Public Health 41:86–90
Ejere VC, Aguzie OI, Ivoke N, Ekeh FN, Ezenwaji NE, Onoja US, Eyo JE (2014) Parasitofauna of five freshwater fishes in a Nigerian freshwater ecosystem. Ribarstvo 72:17–24. https://doi.org/10.14798/72.1.682
El-Dakhly KM, Hussein NM, El-Nahass E (2018) Occurrence of helminths in the great cormorants, Phalacrocorax carbo, in Qena, Egypt. J Adv Vet Anim Res 8:6–11
El-Shahawy IS, El-Seify MO, Metwally AM, Fwaz MM (2017) Survey on endoparasitic fauna of some commercially important fishes of the River Nile, southern of Egypt (Egypt). Rev Med Vet 168:126–134
Ferris FG (1928) The principles of systematic entomology. Stanford University Publications, University Series: Biological Sciences 5:1–169
Galaktionov KV, Dobrovolskij A (2003) The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmissions, and evolution of digenetic trematodes. Springer Science & Business Media, Berlin, p 592
Gustinelli A, Caffara M, Florio D, Otachi EO, Wathuta EM, 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. Sys Parasitol 76:39–51. https://doi.org/10.1007/s11230-010-9231-5
IUCN (2019) The IUCN red list of threatened species. Version 2019-3. http://www.iucnredlist.org
Jhansilakshmibai K, Madhavi R (1997) Euclinostomum heterostomum (Rudolphi, 1809) (Trematoda): life-cycle, growth and development of the metacercaria and adult. Sys Parasitol 38:51–64
Liao XH (1992) The biology of Clinostomum complanatum (Rud.) life history. Wuyi Sci J 9:99–134
Locke SA, Al-Nasiri FS, Caffara M, Drago F, Kalbe M, Lapierre AR, McLaughlin JD, Nie P, Overstreet RM, Souza GTR, Takemoto RM, Marcogliese DJ (2015a) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. Int J Parasitol 45:841–855. https://doi.org/10.1016/j.ijpara.2015.07.001
Locke SA, Caffara M, Marcogliese DJ, Fioravanti ML (2015b) A large-scale molecular survey of Clinostomum (Digenea, Clinostomidae). Zool Scr 44:203–217. https://doi.org/10.1111/zsc.12096
Locke SA, Caffara M, Barčák D, Tedesco P, Fioravanti ML, Li W (2019) A new species of Clinostomum Leidy, 1856 in East Asia based on genomic and morphological data. Par Res 118:3253–3265. https://doi.org/10.1007/s00436-019-06536-y
Maccagno T (1934) Osservazioni intorno a Clinostomum complanatum. Ital J Zool 5:45–60. https://doi.org/10.1080/11250003409426258
Matthews D, Cribb TH (1998) Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni from Egretta intermedia. Sys Parasitol 39:199–208. https://doi.org/10.1023/A:1005982530560
Olivier PAS, Luus-Powell WJ, Saayman JE (2009) Report on some monogenean and clinostomid infestations of freshwater fish and waterbird hosts in Middle Letaba Dam, Limpopo Province, South Africa. Onderstepoort J Vet Res 76:187–199. https://doi.org/10.4102/ojvr.v76i2.44
Ortlepp RJ (1935) On the metacercaria and adult of Clinostomum van der horsti sp. n., a trematode parasite of fishes and herons. Onderstepoort J Vet Sci Animal Ind 5:51–58
Pérez-Ponce de León G, García-Varela M, Pinacho-Pinacho CD, Sereno-Uribe AL, Poulin R (2016) Species delimitation in trematodes using DNA sequences: middle-American Clinostomum as a case study. Parasitology 143:1773–1789. https://doi.org/10.1017/S0031182016001517
Pritchard MH, Kruse G (1982) The collection and preservation of animal parasites. University of Nebraska Press, Lincoln, Nebraska
Rosser TG, Alberson NR, Woodyard ET, Cunningham FL, Pote LM, Griffin MJ (2017) Clinostomum album n. sp. and Clinostomum marginatum (Rudolphi, 1819), parasites of the great egret Ardea alba L. from Mississippi, USA. Sys Parasitol 94:35–49. https://doi.org/10.1007/s11230-016-9686-0
Rosser TG, Baumgartner WA, Alberson NR, Noto TW, Woodyard ET, King DT, Wise DJ, 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 life-cycle stages of Clinostomum album Rosser, Alberson, Woodyard, Cunningham, Pote & Griffin, 2017 in Mississippi, USA. Sys Parasitol 95:543–566. https://doi.org/10.1007/s11230-018-9801-5
Sereno-Uribe AL, Pinacho-Pinacho CD, Garcia-Varela M, Perez-Ponce de Leon 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. Par Res 112:2855–2870. https://doi.org/10.1007/s00436-013-3457-5
Sereno-Uribe AL, García-Varela M, Pinacho-Pinacho CD, Pérez-Ponce de León G (2018) Three new species of Clinostomum Leidy, 1856 (Trematoda) from middle American fish-eating birds. Par Res 117:2171–2185. https://doi.org/10.1007/s00436-018-5905-8
Ukoli FMA (1966a) On Clinostomum tilapiae n. sp., and C. phalacrocoracis Dubois, 1931 from Ghana, and a discussion of the systematics of the genus Clinostomum Leidy, 1856. J Helminthol 40:187–214. https://doi.org/10.1017/S0022149X00034192
Ukoli FMA (1966b) On the life history, growth and development from the metacercarial stage to adulthood, of Clinostomum tilapiae Ukoli, 1966. J Helminthol 40:215–226. https://doi.org/10.1017/S0022149X00034209
Vianna RT, Pereira J Jr, Brandão DA (2003) Ontogenetic variation of metacercariae of Clinostomum complanatum (Rudolphi, 1814) (Digenea: Clinostomidae). Comun Mus Ciênc Tecnol PUCRS Zool 16:223–243.
Acknowledgments
We are grateful for the thoughtful comments provided by reviewers of this communication. We are grateful to Willem J Smit, David Kunutu, and Hendrik Hattingh for assisting with field work in South Africa.
Funding
Work in South Africa by AH was partly supported by the VLIR-IUC (Vlaamse Interuniversitaire Raad – University Development Cooperation) Funding Programme (Belgium) and the South African Research Chairs Initiative (SARChI) of the Department of Science and Technology and National Research Foundation (NRF) of South Africa (Grant No. 101054). SAL received support from the National Science Foundation (1845021).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Applicable international, national, and institutional guidelines for the care and use of animals were followed.
Conflict of interest
The authors declare that they have no conflict of interest.
Disclaimer
Any opinion, finding, and conclusion or recommendation expressed in this material is that of the authors and the NRF does not accept any liability in this regard.
Additional information
Section Editor: Stephen A. Bullard
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Caffara, M., Locke, S.A., Echi, P.C. et al. A new species of Clinostomum Leidy, 1856 based on molecular and morphological analysis of metacercariae from African siluriform fishes. Parasitol Res 119, 885–892 (2020). https://doi.org/10.1007/s00436-019-06586-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06586-2