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An Annotated List and Molecular Data on Larvae ... -.:University of Limpopo Syst Parasitol (2018) 95:567–590 https://doi.org/10.1007/s11230-018-9796-y An annotated list and molecular data on larvae of gryporhynchid tapeworms (Cestoda: Cyclophyllidea) from freshwater fishes in Africa Toma´sˇ Scholz . Sareh Tavakol . Lucie Uhrova´ . Jan Brabec . Iva Prˇikrylova´ . Sˇa´rka Masˇova´ . Andrea Sˇimkova´ . Ali Halajian . Wilmien J. Luus-Powell Received: 20 October 2017 / Accepted: 20 March 2018 / Published online: 16 May 2018 Ó Springer Science+Business Media B.V., part of Springer Nature 2018 Abstract An annotated list of larvae (metacestodes) Fuhrmann, 1912 (1 species), Neogryporhynchus Baer of gryporhynchid tapeworms (Cestoda: Cyclophyl- & Bona, 1960 (1 species), Paradilepis Hsu¨, 1935 (4 lidea) from freshwater fishes in Africa is provided with species), Parvitaenia Burt, 1940 (5 species), and numerous new host and geographical records. Newly Valipora Linton, 1927 (2 species). Additionally, collected materials from Burundi, Democratic Repub- metacestodes of four unidentified species of Para- lic of the Congo, Kenya, Madagascar, Namibia, dilepis and Parvitaenia are reported from fish for the Senegal, South Africa, Sudan and Zimbabwe practi- first time. Rostellar hooks of all species are illustrated cally double the total number of species reported from and their measurements are provided together with a African fish so far. We confirm the occurrence of 16 host-parasite list. The molecular phylogenetic analysis species (five unidentified to the species level and most based on partial LSU rDNA sequences offers the first likely representing new taxa) belonging to the genera insight into the internal phylogenetic relationships Amirthalingamia Bray, 1974 (1 species), Cyclustera within the family. Together with the morphological Fuhrmann, 1901 (2 species), Dendrouterina observations, the present study provides a taxonomic baseline for future studies on this largely neglected, but widely distributed and relatively frequent, group of parasites of African fishes, including economically T. Scholz and S. Tavakol contributed equally. important cichlids like tilapias and cyprinids. This article is part of the Topical Collection Cestoda. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s11230-018-9796-y) con- tains supplementary material, which is available to authorized users. T. Scholz (&) Á L. Uhrova´ Á J. Brabec S. Tavakol Á I. Prˇikrylova´ Á A. Halajian Á Institute of Parasitology, Biology Centre, Czech Academy W. J. Luus-Powell of Sciences, Branisˇovska´ 31, 370 05 Cˇ eske´ Budeˇjovice, Department of Biodiversity, University of Limpopo, Czech Republic Private Bag X1106, Sovenga 0727, South Africa e-mail: [email protected] I. Prˇikrylova´ Á Sˇ. Masˇova´ Á A. Sˇimkova´ L. Uhrova´ Department of Botany and Zoology, Faculty of Science, Department of Parasitology, University of South Bohemia Masaryk University, Kotla´rˇska´ 2, 611 37 Brno, Czech in Cˇ eske´ Budeˇjovice, Branisˇovska´ 31a, Republic 370 05 Cˇ eske´ Budeˇjovice, Czech Republic 123 568 Syst Parasitol (2018) 95:567–590 Introduction recently, Truter et al. (2016) reported, but did not characterise morphologically, the following four Freshwaters of the African continent are inhabited by species from the cichlid Pseudocrenilabrus philander an extraordinarily rich fauna of teleost fishes, hosts of (Weber) in South Africa: Paradilepis scolecina (Ru- numerous groups of parasites including helminths dolphi, 1819); P. maleki Khalil, 1961; Neogry- (Khalil & Polling, 1997). Some helminths of African porhynchus lasiopeius Baer & Bona, 1960; and fishes have been studied relatively intensively, espe- Valipora campylancristrota (Wedl, 1855). Therefore, cially monogeneans of cichlids, including the eco- a total of eight species of six genera were known, but nomically important tilapias (e.g. Vanhove et al., 2016 not characterised in detail, from African freshwater and references therein). In contrast, some groups of fishes before the present study. metazoan fish parasites remain completely neglected, The main goal of the present account is to provide a such as the larvae (metacestodes) of gryporhynchid robust taxonomic baseline necessary for future tapeworms (Cestoda: Cyclophyllidea). research on this almost completely neglected, but Adult tapeworms of the family Gryporhynchidae relatively frequently occurring group of fish parasites. Spassky & Spasskaya, 1973 are intestinal parasites of The present study also appeals to fish parasitologists fish-eating birds, especially herons, storks, cormorants and veterinarians for much more attention to be paid to and ibises (Baer & Bona, 1960). They were previously gryporhynchid larvae, which are relatively common in placed in the Dilepididae (see Bona, 1975, 1994), but several African fishes such as cichlids, including the are currently recognised as a separate family within economically important tilapias, but whose biology, the Cyclophyllidea (see Caira & Jensen, 2017; Mari- species diversity, distribution and associations with aux et al., 2017). their fish hosts remain poorly known. The systematics and diversity of gryporhynchids parasitising fish-eating birds of the Order Ciconi- iformes were reviewed by Bona (1975), who reported Materials and methods adults of 19 species to occur in Africa, but did not provide any data on gryporhynchid larvae in African The present review is based on taxonomic evaluation fishes. The first record of metacestodes of gry- of extensive material of gryporhynchid larvae porhynchids from African fishes was published by (metacestodes) recently collected by the authors and Bray (1974), who found larvae of Amirthalingamia their collaborators from a range of fish species macracantha (Joyeux & Baer, 1935) in Oreochromis throughout Africa (Burundi, Kenya, Madagascar, niloticus (L.). Khalil & Polling (1997) reported larvae Namibia, Senegal, South Africa, Sudan and Zim- of only two species of gryporhynchids identified to the babwe; see Supplementary file for a list of material species level, i.e. A. macracantha and Paradilepis studied). To better observe the hooks, some specimens delachauxi (Fuhrmann, 1909). In addition, larvae of an were flattened under a coverslip and fixed in glycerine unidentified species of Anomotaenia Cohn, 1900 and ammonium picrate solution (GAP) following the ‘dilepidid’ larvae were reported from tilapias (Khalil method of Malmberg (1957) and Ergens (1969) used & Polling, 1997). for studies of sclerotised parts of monogeneans. In a review of gryporhynchid metacestodes in Because of large number of larvae in some fish, other fishes, Scholz et al. (2004) listed only two species from larvae were fixed in 70% or 96% ethanol. Some of the Africa, namely A. macracantha and Cyclustera magna former specimens were stained with Mayer’s carmine, (Baer, 1959). Later, Scholz et al. (2008) reported dehydrated and mounted as permanent preparations. Parvitaenia samfyia Mettrick, 1967 and Cyclustera sp. Samples fixed in 99% molecular-grade ethanol from the common carp, Cyprinus carpio L., a non- were used for DNA extraction and sequencing of the native fish introduced to Africa for aquaculture. Most partial (domain D1–D3) nuclear large subunit of the ribosomal RNA gene (LSU rDNA). The molecular dataset was generated within the scope of the BSc I. Prˇikrylova´ Water Research Group, Unit for Environmental Sciences thesis of one of the authors (LU) following the and Management, North-West University, methodology described in Brabec et al. (2012). Private Bag X6001, Potchefstroom 2520, South Africa Individual Sanger reads were assembled and checked 123 Syst Parasitol (2018) 95:567–590 569 for errors in Geneious 8.1.7. (Kearse et al., 2012). Syns Dilepis delachauxi Joyeux & Baer, 1930, nec Contiguous sequences were aligned using the E-INS-i Fuhrmann, 1909; Paradilepis macracantha Joyeux & algorithm of the program MAFFT (Katoh & Standley, Baer, 1935; Amirthalingamia sp. of Aloo (2002) 2013); ambiguously aligned positions were manually excluded and phylogenetic analyses run under the Type-host: Microcarbo africanus (Gmelin) (syn. Pha- maximum likelihood criterion using the program lacrocorax africanus) (Suliformes: Phalacrocoraci- PHYML (Guindon et al., 2010); all within the dae), long-tailed cormorant. Geneious program environment. The best tree search Type-locality: Mali. employed the GTR?I?C model of nucleotide evolu- Fish hosts: Coptodon zillii (Gervais), *Pharyn- tion and subtree pruning and regrafting branch gochromis acuticeps (Steindachner) (1 of 2 fish from swapping. Zimbabwe infected), *Pseudocrenilabrus philander In addition, search of the literary data published (2/8; Zimbabwe), *Tilapia sparrmanii Smith (1/6; since 2004, i.e., after the review by Scholz et al. Zimbabwe) (all Perciformes: Cichlidae); ‘catfish’ (2004), was carried out. Voucher specimens of larvae (Siluriformes). studied were deposited in the Helminthological Col- Site in host: Liver, body cavity, intestinal wall. lection of the Institute of Parasitology, Biology Centre Geographical distribution of larvae: *Democratic of the Czech Academy of Sciences, Cˇ eske´ Budeˇjovice, Republic of the Congo, Kenya, *Zimbabwe; adults Czech Republic (IPCAS); Collection of Platy- were found in Mali and the Sudan. helminthes at the Natural History Museum, Geneva, Voucher specimens: IPCAS C-292/1–3; NHMUK Switzerland (MHNG-PLAT); Parasite Collection of 1985.1.7.24. the Natural History Museum, London, UK (acronym Representative DNA sequences: Sequences from NHMUK); the Royal Museum of Central Africa, specimens ex P. philander (MH062173;
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