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. 2018 Jan 27;55(1):84–87. doi: 10.1515/helm-2017-0052

The First Record of the Invasive Asian Fish Tapeworm (Schyzocotyle Acheilognathi) from An Endemic Cichlid Fish in Madagascar

T Scholz 1,*, A Šimková 2,*, J Rasamy Razanabolana 3,*, R Kuchta 1,*
PMCID: PMC6799532  PMID: 31662631

Summary

The Asian fish tapeworm, Schyzocotyle acheilognathi (Yamaguti, 1934) (Cestoda: Bothriocephalidea), is an invasive parasite of freshwater fishes that have been reported from more than 200 freshwater fish worldwide. It was originally described from a small cyprinid, Acheilognathus rombeus, in Japan but then has spread, usually with carp, minnows or guppies, to all continents including isolated islands such as Hawaii, Puerto Rico, Cuba or Sri Lanka. In the present account, we report the first case of the infection of a native cichlid fish, Ptychochromis cf. inornatus (Perciformes: Cichlidae), endemic to Madagascar, with S. acheilognathi. The way of introduction of this parasite to the island, which is one of the world’s biodiversity hotspots, is briefly discussed.

Keywords: Invasive parasite, new geographical record, Cestoda, Cichlidae, Madagascar

Introduction

Madagascar is a biodiversity hotspot with over 90 % of its fauna represented by endemic species (Hobbes & Dolan, 2008). Even though the island is situated near the African continent, it originally belonged to the Indian Peninsula, from which it split around 88 million years ago (Rosemary & Clague, 2009). The island’s diverse ecosystems and unique wildlife are threatened by the encroachment of the rapidly growing human population and other environmental threats, including water pollution (Benstead et al., 2003). As much as 41 % (71 from 172) species of freshwater fish from Madagascar are endemic, including two endemic families (Froese & Pauly, 2017). Native fish are also endangered by the introduction of non-native fish species and their parasites, which may have a detrimental effect on local fish communities, especially of native hosts, which are not adapted to these newly introduced parasites (Lévêque, 1997).

One of the most widely distributed fish parasites, and probably the most successful invasive parasite at all, is the so called Asian fish tapeworm, Schyzocotyle acheilognathi (Yamaguti, 1934) (syn. Bothriocephalus acheilognathi) (Cestoda: Bothriocephalidea). This tapeworm of the supposedly East Asian origin has been reported from more than 200 species of freshwater fish throughout the world, including isolated islands such as the Hawaii, Puerto Rico, Cuba or Sri Lanka (Font, 2003; Choudhury et al., 2006; Scholz et al., 2012).

The parasite has been disseminated worldwide mainly due to the import of veterinary uninspected common carp, grass carp, guppies and minnows (Scholz et al., 2012). It may reduce the growth of fish fry or even cause mortality, as reported in the 1960’ – 1980’s in the former USSR and central Europe (Bauer et al., 1973; Scholz, 1999). However, it also represents a threat for populations of native fish (Williams & Jones, 1994; Dove et al., 1997).

Material and Methods

In April 2016, freshwater fishes of six species from Antsohihy (Anjingo River), Madagascar (14°53’ S, 47°54’ E) were examined for the presence of metazoan parasites. Among them, originally unidentified species of the endemic cichlid genus Ptychochromis Steindachner, 1880, designated as Ptychochromis sp. 1 (Perciformes: Cichlidae; field nos. 18/1; 19/2; 21/4; 22/5; 30/11; 32/13), was infected with 43 specimens of S. acheilognathi (prevalence 40 %; intensity of infection 1 – 18; mean intensity ± SD 7.5 ± 8.2; mean abundance ± SD 3.0 ± 6.2).

Tapeworms were fixed in 70 % ethanol under pressure (for morphological evaluation) and in 96 % molecular-grade ethanol (for DNA sequencing). The specimens fixed with 70 % ethanol were stained with Mayer’s carmine, dehydrated in an ethanol series, cleared with clove oil and mounted in Canada balsam; they were deposited as vouchers at the Helminthological Collection of the Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic (IPCAS C-15/35).

Partial cox1 gene of one of the specimens was sequenced by J. Brabec using the method described by Brabec et al. (2016). We analyzed a segment (580 bp) of DNA from the mitochondrial large ribosomal subunit (16S) of RNA gene for our Ptychochromis sp. 1 using the same primers as applied for Malagasy and South African cichlids by Sparks and Smith (2004). The obtained DNA sequence was identical with the sequence of Ptychochromis inornatus from GenBank (accession number AY263876). Therefore, the host is designated as Ptychochromis cf. inornatus. The PCR conditions and methods followed Mendlová et al. (2012).

Results and Discussion

Tapeworms found in Ptychochromis cf. inornatus (Fig. 1A) belong to the family Bothriocephalidae because they possess median gonopores (a dorsally situated common cirro-vaginal pore and a ventral uterine pore) (Kuchta et al., 2008; Brabec et al., 2015). They were identified as S. acheilognathi based on the typical heart-shaped scolex bearing deep and narrow bothria with slit-like orifices (Fig. 1B; Pool & Chubb, 1985). Most tapeworms were not fully developed and only a few specimens contained gravid proglottids with the eggs in the uterus. Species identification was confirmed by the cox1 gene sequence, which corresponds to that of S. acheilognathi (J. Brabec – unpubl. data; see also Brabec et al., 2015, 2016).

Fig. 1.

Fig. 1

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A – Ptychochromis cf. inornatus from Madagascar, definitive host of Schyzocotyle acheilognathi (Yamaguti, 1934) B – Anterior part of S. acheilognathi with scolex.

None of the five other fish species examined including one native and endemic species, Paretroplus lamenabe Sparks, 2008 (Cichlidae), three native species, namely Pachypanchax omalonotus (Duméril, 1861) (Aplocheilidae), Valamugil robustus (Günther, 1861) (Mugilidae) and Glossogobius giuris (Hamilton, 1822) (Gobiidae), and one introduced species, Oreochromis niloticus (Linnaeus, 1758) (Cichlidae), were infected by this parasite.

Schyzocotyle acheilognathi has been reported from 9 countries of Africa including Morocco (new geographical and host records from Carasobarbus fritchii (Günther, 1874), Luciobarbus massaensis (Pellegrin, 1922), L. rifensis Doadrio, Casal-Lopez & Yahyaoui, 2015, L. yahyaouii Doadrio, Casal-López & Perea, 2016 and L. rabatensis Doadrio, Perea & Yahyaoui, 2015 – unpublished data of the present authors). However, no data on its occurrence in Madagascar are available (Gibson et al., 2005; Kuchta et al., 2012).

The origin and the way of the introduction of S. acheilognathi to this island remains unclear, even though a number of alien fish species have been introduced to Madagascar (Kiener, 1963). Many fish were introduced for aquaculture and others to improve fish production in natural water bodies. However, breeding fish often escaped from fishponds and succeeded well in wild habitats. The first two fish species, Osphronemus gouramy Lacépède and Carassius auratus (Linnaeus), were introduced to Madagascar from East Asia and Europe (France) in 1857 and 1861, respectively (Kiener, 1963). Common carp (Cyprinus carpio Linnaeus), which is one of the most susceptible definitive hosts of S. acheilognathi, was imported from France to Madagascar in 1916. From 1966 to 1972, juveniles of common carp were reintroduced into Lake Alaotra. In the 1950’s and 1960’s, several species of tilapias were also introduced (Kiener, 1963), but S. acheilognathi has never been reported from any of the introduced or native fish (Khalil & Polling, 1997; Gibson et al., 2005; R. Kuchta – unpubl. data).

Cichlids and perciform fishes in general are not the most common definitive hosts of S. acheilognathi. A total of 12 species of perciform fish (out of more than 200 fish species) were previously reported as hosts of S. acheilognathi, mostly from Mexico, with two records from Oreochromis niloticus (Linnaeus) in South Africa and Nigeria (Paperna, 1996; Ogbulie et al., 2011).

Conclusion

The present report of S. acheilognathi from Madagascar, which is a new geographical and host record of this invasive parasite, is considered to be of concern from the veterinary and conservation point of view, especially because this parasite was found in an endemic fish and with a high prevalence and intensity of infection. Even though the pathological effect of S. acheilognathi on cichlid fishes has not been studied, the observed infection rate indicates that this tapeworm has successfully colonized a new region, an isolated island in the Indian Ocean, most probably as a result of human activities. Therefore, inspection of cichlids and other fishes from the locality and surrounding water bodies is strongly recommended to detect possible spreading of this invasive and potentially dangerous fish parasite.

Acknowledgements

The authors are much obliged to J. Brabec, Institute of Parasitology, BC CAS, České Budějovice, for providing unpublished sequence of S. acheilognathi from Madagascar, J. R. Rasoloariniaina, Centre National de Recherche sur l’Environnement, Antananarivo, for help in capturing fish and species determination, Eva Řehulková and Maarten P.M. Vanhove for the help with fish dissection and parasite collection. Financial support of the Czech Science Foundation (projects Nos. P505/12/G112 and 15-14198-S) and the Institute of Parasitology (RVO: 60077344) is also acknowledged. An anonymous reviewer provided helpful suggestions.

Footnotes

1

This fixation method, i.e. flattening of tapeworms and their fixation in 70 %, is not recommended; instead, heat-fixation, best with 4 % hot formaldehyde solution, should be used – see, e.g., Oros et al. (2010).

References

  1. BAUER O.N., MUSSELIUS V.A., STRELKOV Y.A. Diseases of Pond Fishes. Jerusalem, Israel: Israel Programme for Scientific Translations; 1973. p. 220. [Google Scholar]
  2. BENSTEAD J.P., DE RHAM P.H GATTOLLIAT, J.-L., GIBON F.-M., LOISELLE P.V., SARTORI M., SPARKS J.S STIASSNY, M.L.J.. Conserving Madagascar’s freshwater biodiversity. BioScience. 2003;53:1101–1111. doi: 10.1641/0006-3568(2003)053[1101:CMFB]2.0.CO;2. [DOI] [Google Scholar]
  3. BRABEC J., KUCHTA R., SCHOLZ T., LITTLEWOOD D.T.J.. Paralogues of nuclear ribosomal genes conceal phylogenetic signal within the invasive Asian fish tapeworm lineage: evidence from next generation sequencing data. Int. J. Parasitol. 2016;46:555–562. doi: 10.1016/j.ijpara.2016.03.009. [DOI] [PubMed] [Google Scholar]
  4. BRABEC J., WAESCHENBACH A., SCHOLZ T., LITTLEWOOD D.T.J., KUCH-TA R.. Molecular phylogeny of the Bothriocephalidea (Cestoda): molecular data challenge morphological classification. Int. J. Parasitol. 2015;45:761–771. doi: 10.1016/j.ijpara.2015.05.006. [DOI] [PubMed] [Google Scholar]
  5. CHOUDHURY A., CHARIPAR E., NELSON P., HODGSON J.R., BONAR S., COLE R.A.. Update on the distribution of the invasive Asian fish tapeworm, Bothriocephalus acheilognathi in the U.S. and Canada. Comp. Parasitol. 2006;73:269–273. doi: 10.1654/4240.1. doi: 10.1654/4240.1. DOVE, A.D.M., CRIBB, T.H., MOCKLER, S.P., LINTERMANS, M. (1997): The Asian fish tapeworm, Bothriocephalus acheilognathi in Australian freshwater fishes. Mar. Freshw. Res 48: 181–183. [DOI] [Google Scholar]
  6. FONT W. F.. The global spread of parasites: what do Hawaiian streams tell us? Bioscience. 2003;53:1061–1067. [Google Scholar]
  7. GIBSON D.I., BRAY R.A., HARRIS E.A. Host-Parasite Database of the Natural History Museum, London. World Wide Web electronic publication. 2005. http://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/ Compilers.
  8. HOBBES J., DOLAN A. World Regional Geography 6th edition. Belmont, California, USA: Cengage Learning; 2008. p. 752. [Google Scholar]
  9. KHALIL L.F., POLLING L. Check List of the Helminth Parasites of African Freshwater Fish. Pietersburg: South Africa, University of the North; 1997. p. 185. 2nd edition. [Google Scholar]
  10. KIENER A.. Poissons, pêche et pisciculture à Madagascar. Publ. Centre Techn. For. Trop. 1963;24:244. pp. [Google Scholar]
  11. KUCHTA R., BURIANOVÁ A., JIRKŮ M., DE CHAMBRIER A., OROS M., BRABEC J., SCHOLZ T.. Bothriocephalidean tapeworms (Cestoda) of freshwater fish in Africa, including erection of Kirstenella n. gen. and description of Tetracampos martinae n. sp. Zootaxa. 2012;3309:1–35. [Google Scholar]
  12. KUCHTA R., SCHOLZ T., BRAY R.A.. Revision of the order Bothriocephalidea Kuchta, Scholz, Brabec & Bray, 2008 (Eucestoda) with amended generic diagnoses and keys to families and genera. Syst. Parasitol. 2008;71:81–136. doi: 10.1007/s11230-008-9153-7. [DOI] [PubMed] [Google Scholar]
  13. LÉVÊQUE C. Biodiversity Dynamics and Conservation: The Freshwater Fish of Tropical Africa. Cambridge, UK: Cambridge University Press; 1997. p. 438. [Google Scholar]
  14. MENDLOVÁ M, DESDEVISES Y, CIVÁŇOVÁ K, PARISELLE A, ŠIMKOVÁ A.. Monogeneans of West African cichlid fish: evolution and cophylogenetic interaction. PLoS ONE. 2012;7:e37268. doi: 10.1371/journal.pone.0037268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. OGBULIE T.E., NWIGWE H.C., ANYADOH S.O.. Comparative assessment of bioload of healthy and diseased Oreochromis niloticus as means of food security. Anal. Univ. Oradea, Fasc. Biol. 2011;18:10–14. [Google Scholar]
  16. OROS M., SCHOLZ T., HANZELOVÁ V., MACKIEWICZ J.S.. Scolex morphology of monozoic cestodes (Caryophyllidea) from the Palaeartctic Region: a useful tool for species identification. Folia Parasitol. 2010;57:37–46. doi: 10.14411/fp.2010.006. [DOI] [PubMed] [Google Scholar]
  17. PAPERNA I. Parasites, Infections and Diseases of Fishes in Africa: An Update. CIFA Technical Paper; 1996. [Google Scholar]
  18. POOL D.W., CHUBB J.C.. A critical scanning electron microscope study of the scolex of Bothriocephalus acheilognathi Yamaguti, 1934, with a review of the taxonomic history of the genus Bothriocephalus parasitizing cyprinid fishes. Syst. Parasitol. 1985;7:199–211. doi: 10.1007/BF00011451. [DOI] [Google Scholar]
  19. ROSEMARY G.G., CLAGUE D.A.. Encyclopedia of Islands. Berkeley, USA, University of California Press, 1075 pp. SCHOLZ, T. (1999): Parasites in cultured and feral fish. Vet. Parasitol. 2009;84:317–335. doi: 10.1023/A:1006120500518. [DOI] [PubMed] [Google Scholar]
  20. SCHOLZ T., KUCHTA R., WILLIAMS C. WOO P.T.K., BUCHMANN K. Fish Parasites. Pathobiology and Protection Chapter 18. Wallingford, UK: CAB International; 2012. Bothriocephalus achelognathi; pp. 282–297. [Google Scholar]
  21. SPARKS J.S., SMITH W.L.. Molecular phylogeny and biogeography of the Malagasy and South Asian cichlids (Teleostei: Perciformes: Cichlidae) Mol. Phyl. Evol. 2004;30:599–614. doi: 10.1016/j.ympev.2004.07.002. [DOI] [PubMed] [Google Scholar]
  22. WILLIAMS H.H., JONES A. Parasitic Worms of Fishes. London & Bristol, UK, Taylor & Francis: 1994. p. 593. [Google Scholar]

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