Abstract
The monogenean genus Heterobothrium (Monogenea: Diclidophoridae) currently consists of 12 accepted species described globally from various pufferfishes (Tetraodontidae). This includes the economically important Heterobothrium okamotoi Ogawa 1991 that causes severe disease in the cultured tiger puffer Takifugu rubripes in Japan. During parasitological surveys targeting near shore marine fishes of South Africa, a new Heterobothrium was discovered on the gills of five evileye pufferfish Amblyrhynchotes honckenii with a prevalence of 100% and mean intensity of 23 (4–72). Specimens were morphologically studied using both light and scanning electron microscopy and molecularly characterized by sequencing the partial ribosomal gene 28S. Heterobothrium victorwepeneri n. sp. differs from its 12 congeners by a combination of morphological characters, such as fourth clamp pair (anteriormost, 180° inverted) as the smallest with some of the sclerites differing in shape from the other pairs, 8 to 9 genital hooks, number of testes 40–50, and absent isthmus. The 28S tree depicted two main branches, one clustering together species of mazocraeidean families while the other clustered together only species of the Diclidophoridae. Heterobothrium victorwepeneri n. sp. is the first species of its genus to be recorded and described from South Africa and from the tetraodontid A. honckenii. This study also provides for the first time 28S sequence for a species of this highly host-specific genus.
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References
Blasco-Costa I, Cutmore SC, Miller TL, Nolan MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Syst Parasitol 93:295–306. https://doi.org/10.1007/s11230-016-9631-2
Bray RA (1986) Some helminth parasites of marine fishes of South Africa: families Enenteridae, Opistholebetidae and Pleorchiidae (Digenea). J Nat Hist 20:471–488
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583
Bychowsky BE, Mamaev-Yu L, Nagibina, LF (1976) Revision of the genus Heterobothrium Cerfontaine, 1895 (Diclidophoridae). Trudy-Biologo-Pochvennogo-Instituta-Issledovaniya-monogenticheskikh-sosal’shchikov,-Novaya-Seriya 34:29–40
Desdevises Y, Morand S, Legendre P (2002) Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea). Biol J Linn Soc 77:431–443. https://doi.org/10.1046/j.1095-8312.2002.00114.x
Ergens R (1969) The suitability of ammonium picrate-glycerin in preparing slides of lower Monogenoidea. Folia Parasitol 16:320
Euzet L, Birgi E (1975) Heterobothrium fluviatilis n. sp. (Monogenea, Diclidophoridae), gill parasite of Tetraodon fahaka Bennett 1834 (Teleostei) in Chad. Bull Soc Zool Fr 100:411–420
Froese R, Pauly D (2020) FishBase. World Wide Web electronic publication. www.fishbase.org/search.php
Goto S (1894) Studies on the ectoparasitic trematodes from Japan. J Coll Sci Imp Univ Tokyo 8:1–273
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. https://doi.org/10.1080/10635150390235520
Hadfield KA, Bruce NL, Smit NJ (2010) Redescription of the monotypic genus Cinusa Schioedte and Meinert, 1884 (Isopoda, Cymothoidae), a buccal-cavity isopod from South Africa. Zootaxa 2437:51–68. https://doi.org/10.5281/zenodo.194854
Kearn GC (1998) Parasitism and the Platyhelminthes. Chapman and Hall, London
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lisitsyna OI, Kudlai O, Cribb TH, Smit NJ (2019) Three new species of acanthocephalans (Palaeacanthocephala) from marine fishes collected off the East Coast of South Africa. Folia Parasitologica 66:012. https://doi.org/10.14411/fp.2019.012
Littlewood DTJ, Rohde K, Clough KA (1997) Parasite speciation within or between host species: phylogenetic evidence from site-specific polystome monogeneans. Int J Parasitol 27:1289–1297
Littlewood DTJ, Curini-Galletti M, Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466. https://doi.org/10.1006/mpev.2000.0802
Lockyer AE, Olson PD, Littlewood DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 78:155–171. https://doi.org/10.1046/j.1095-8312.2003.00141.x
Malmberg G (1956) Skrifer utgivna av Södra Sveriges Fiskeriförening. Arsskr:19–76
Meserve FGC (1938) Some monogenetic trematodes from Galapagos Islands and the neighbouring Pacific. Allan Hancock Pacific Expedition 2:31–89
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. SC10 Workshop on Gateway Computing Environments (GCE10), New Orleans, Louisiana, 14 November 2010, pp. 1–8. https://doi.org/10.1145/2016741.2016785
Mollaret I, Jamieson BGM, Adlard RD, Hugall A, Lecointre G, Chombard C, Justine JL (1997) Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from the 28S rDNA sequences. Mol Biochem Parasit 90:433–438. https://doi.org/10.1016/s0166-6851(97)00176-x
Morsy K, Saady H, Abdel-Ghaffar F, Bashtar A-R, Mehlhorn H, Quraishy SA, Adel A (2012) A new species of the genus Heterobothrium (Monogenea: Diclidophoridae) parasitizing the gills of tiger puffer fish Tetraodon lineatus (Tetraodontidae). A light and scanning electron microscopic study. Parasitol Res 110:1119–1124. https://doi.org/10.1007/s00436-011-2601-3
Nagibina LF (1953) Heterobothrium affinis (Linton) and its position in the systematics of monogenetic trematodes of the family Diclidophoridae (Fuhrmann). Zoological Institute of Academy of Sciences USSR XIII:137–143
Ogawa K (1991) Redescription of Heterobothrium tetrodonis (Goto, 1894) (Monogenea: Diclidophoridae) and other related new species from puffers of the genus Takifugu (Teleostei: Tetraodontidae). Jpn J Parasitol 40:388–396
Ogawa K (2002) Impacts of diclidophorid monogenean infections on fisheries in Japan. Int J Parasitol 32:373–380. https://doi.org/10.1016/S0020-7519(01)00338-1
Oliva ME, Sepulvida FA, González MT (2014) Parapedocotyle prolatili gen. n. et sp. n., a representative of the Diclidophoridae (Monogenea), a gill parasite of Prolatilus jugularis (Teleostei: Pinguipedidae) from Chile. Folia Parasitol 61:543–548. https://doi.org/10.14411/fp.2014.067
Olson PD, Littlewood DTJ (2002) Phylogenetics of the Monogenea – evidence from a medley of molecules. Int J Parasitol 32:233–244. https://doi.org/10.1016/S0020-7519(01)00328-9
Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg P, Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol 48:369–371. https://doi.org/10.1016/j.ympev.2008.03.024
Poulin R (1992) Determinants of host-specificity in parasites of freshwater fishes. Int J Parasitol 22:753–758. https://doi.org/10.1016/0020-7519(92)90124-4
Rambaut (2009) Molecular evolution, phylogenetics and epidemiology: Fig-Tree. World Wide Web electronic publication. http://tree.bio.ed.ac.uk/software/figtree/, 07/2018
Ronquist F, Teslenko FM, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget SB, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Schaeffner BC, Smit NJ (2019) Parasites of cartilaginous fishes (Chondrichthyes) in South Africa – a neglected field of marine science. Folia Parasitol 66:002. https://doi.org/10.14411/fp.2019.002
Šimková A, Kadlec D, Gelnar M, Morand S (2002) Abundance-prevalence relationship of gill congeneric ectoparasites: testing the core satellite hypothesis and ecological specialization. Parasitol Res 88:682–686. https://doi.org/10.1007/s00436-002-0650-3
Šimková A, Verneau O, Gelnar M, Morand S (2006) Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution 60:1023–1037. https://doi.org/10.1111/j.0014-3820.2006.tb01180.x
Smit NJ, Davies AJ (2001) An encapsulated haemogregarine from the evileye pufferfish in South Africa. J. Mar. Biol. Assoc. U.K. 81:751–754. https://doi.org/10.1017/S0025315401004556
Smit NJ, Davies AJ (2005) Intraerythrocytic merogony in Haemogregarina koppiensis (Apicomplexa: Adeleorina: Haemogregarinidae). Folia Parasitol 52:277–278. https://doi.org/10.14411/fp.2005.037
Smit NJ, Hadfield KA (2015) Marine fish parasitology in South Africa: history of discovery and future direction. Afr Zool 50:79–92. https://doi.org/10.1080/15627020.2015.1043644
Tambireddy N, Gayatri T, Gireesh-Babu P, Pavan-Kumar A (2016) Molecular characterization and phylogeny of some mazocraeidean monogeneans from carangid fish. Acta Parasitol 61:360–368. https://doi.org/10.1515/ap-2016-0047
Vidal-Martínez VM, Mendoza-Franco EF (2008) Heterobothrium lamothei n. sp. (Monogenea: Diclidophoridae) from the gills of Sphoeroides testudineus (Pisces: Tetraodontidae) from the coast of Yucatán, Mexico. Rev Mex Biodivers 79:89S–93S. https://doi.org/10.7550/rmb.5393
Whittington ID, Crib BW, Hamwood TE, Halliday JA (2000) Host-specificity of monogenean (Platyhelminthes) parasites: a role for anterior adhesive areas? Int J Parasitol 30:305–320. https://doi.org/10.1016/S0020-7519(00)00006-0
Williams A (1986) Taxonomy of two new species of Heterobothrium (Monogenea: Diclidophoridae) from Torquigener pleurogramma (Pisces: Tetraodontidae) from Western Australia. Aust J Zool 34:707–715
Acknowledgements
Mrs. Anja Erasmus, Miss Anja Vermaak, Dr. Wynand Malherbe, and Dr. Kerry Hadfield, NWU-Water Research Group, are thanked for their assistance in the field, and Mr. Willem Landman, NWU African Amphibian Conservation Research Group, is thanked for aiding with the scanning electron microscopy. The authors are also thankful to Eva Řehulková and Kateřina Francová, Faculty of Science, Masaryk University, Brno, Czechia; Edgar Mendoza-Franco, Universidad Autónoma de Campeche, Instituto de Ecología, Pesquerías y Oceanografía del Golfo de México (EPOMEX); Luis García Prieto, Universidad Nacional Autónoma de México; and Kazuo Ogawa, Meguro Parasitological Museum, Tokyo, Japan, for providing relevant literature. The authors are deeply grateful to Tomáš Scholz, Blanka Škoríková, and Camila Pantoja, Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czechia, for providing the photomicrographs of H. lamothei; Anna Hara, Western Australian Museum, Welshpool, Australia, for providing the photomicrographs of H. torquigeneri; and Kazuo Ogawa, Meguro Parasitological Museum, Tokyo, Japan, for providing the photomicrographs of H. shinagawai and H. yamagutii. Three anonymous reviewers are acknowledged for their valuable corrections and comments. This is contribution #480 from the NWU-Water Research Group.
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AAA received postdoctoral funding from the NWU.
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Acosta, A.A., Smit, N.J. A first for Southern Africa: description of a new Heterobothrium (Monogenea: Diclidophoridae) parasitizing the evileye pufferfish Amblyrhynchotes honckenii (Tetraodontiformes: Tetraodontidae). Parasitol Res 120, 819–830 (2021). https://doi.org/10.1007/s00436-020-06960-5
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DOI: https://doi.org/10.1007/s00436-020-06960-5