Hostname: page-component-7479d7b7d-q6k6v Total loading time: 0 Render date: 2024-07-08T21:44:59.412Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphometric and molecular analyses of Tylodelphys sp. metacercariae (Digenea: Diplostomidae) from the vitreous humour of four fish species from Lake Naivasha, Kenya

Published online by Cambridge University Press:  01 April 2014

E.O. Otachi ,
S.A. Locke ,
F. Jirsa ,
C. Fellner-Frank  and
D.J. Marcogliese
E.O. Otachi
Affiliation:
University of Vienna, Department of Integrative Zoology, Althanstrasse 14, 1090Vienna, Austria Egerton University, Biological Sciences Department, PO Box 536, Egerton, Kenya
S.A. Locke
Affiliation:
Aquatic Biodiversity Section, Watershed Hydrology and Ecology Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment Canada, 105 McGill Street, Montreal, QC H2Y 2E7Canada Biodiversity Institute of Ontario, University of Guelph, 50 Stone Road East, Guelph, ON N1G 2W1Canada
F. Jirsa*
Affiliation:
University of Vienna, Institute of Inorganic Chemistry, Althanstrasse 14, 1090Vienna, Austria University of Johannesburg, Department of Zoology, PO Box 524, Auckland Park, 2006South Africa
C. Fellner-Frank
Affiliation:
University of Vienna, Department of Integrative Zoology, Althanstrasse 14, 1090Vienna, Austria
D.J. Marcogliese
Affiliation:
Aquatic Biodiversity Section, Watershed Hydrology and Ecology Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment Canada, 105 McGill Street, Montreal, QC H2Y 2E7Canada
*
* Fax: +43 1 4277 526 20 E-mail: franz.jirsa@univie.ac.at
Get access Rights & Permissions [Opens in a new window]

Abstract

Even in the relatively well-characterized faunas of the developed world, it is difficult to discriminate species of metacercariae in the Diplostomidae using morphology, infection site or host use. The taxonomy, diversity and ecology of diplostomids infecting freshwater fishes in the African continent are particularly poorly known, but recent morphometric and genetic studies have revealed four species of diplostomids in the eyes and brains of siluriform fishes. In the present study, diplostomid metacercariae were collected from the eyes of 288 fish comprising two species within the Cyprinidae (Cyprinus carpio, n= 145, and Barbus paludinosus, n= 67), two Cichlidae (Oreochromis leucostictus, n= 56, and Tilapia zillii, n= 18) and one Centrarchidae (Micropterus salmoides, n= 2) caught in Lake Naivasha, Kenya. Morphometric (14 characters and 8 indices in 111 specimens) and molecular (sequences from the barcode region of the cytochrome c oxidase 1 gene in 11 specimens) data were used to discriminate species. All fish species except B. paludinosus were infected with Tylodelphys metacercariae that were initially separated into two types differing mainly in body length. However, this morphological distinction received only intermediate support in quantitative morphological analysis and molecular data indicated that both morphotypes were conspecific. All the specimens therefore are inferred to belong to a single unidentified species of Tylodelphys, which is not conspecific with any other diplostomid for which comparable molecular data are available, including four diplostomid species known from siluriform fish in Nigeria and Tanzania.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 4 , July 2015 , pp. 404 - 414
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Avise, J. (1994) Molecular markers, natural history and evolution. 511 pp. New York, Chapman and Hall.CrossRefGoogle Scholar
Barnard, P.C. & Biggs, J. (1988) Macroinvertebrates in the catchment streams of Lake Naivasha, Kenya. Revue d'Hydrobiologie Tropicale 21, 127–134.Google Scholar
Behrmann-Godel, J. (2013) Parasite identification, succession and infection pathways in perch fry (Perca fluviatilis): new insights through a combined morphological and genetic approach. Parasitology 140, 509–520.CrossRefGoogle ScholarPubMed
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Campbell, L.M., Osano, O., Hecky, R.E. & Dixon, D.G. (2003) Mercury in fish from three Rift Valley lakes (Turkana, Naivasha and Baringo), Kenya, East Africa. Environmental Pollution 125, 281–286.CrossRefGoogle ScholarPubMed
Cavaleiro, F.I., Pina, S., Russell-Pinto, F., Rodrigues, P., Formigo, N.E., Gibson, D.I. & Santos, M.J. (2012) Morphology, ultrastructure, genetics, and morphometrics of Diplostomum sp. (Digenea: Diplostomidae) metacercariae infecting the European flounder, Platichthys flesus (L.) (Teleostei: Pleuronectidae), off the northwest coast of Portugal. Parasitology Research 110, 81–93.CrossRefGoogle ScholarPubMed
Chappell, L.H. (1995) The biology of diplostomatid eyeflukes of fishes. Journal of Helminthology 69, 97–101.CrossRefGoogle ScholarPubMed
Chappell, L.H., Hardie, L.J. & Secombes, C.J. (1994) Diplostomiasis: the disease and host–parasite interactions. pp. 59–86in Pike, A.W. & Lewis, J.W. (Eds) Parasitic diseases of fish. Tresaith, Dyfed, UK, Samara Publishing.Google Scholar
Chibwana, F.D. & Nkwengulila, G. (2010) Variation in the morphometrics of diplostomid metacercariae (Digenea: Trematoda) infecting the catfish, Clarias gariepinus in Tanzania. Journal of Helminthology 84, 61–70.CrossRefGoogle ScholarPubMed
Chibwana, F.D., Blasco-Costa, I., Georgieva, S., Hosea, K.M., Nkwengulila, G., Scholz, T. & Kostadinova, A. (2013) A first insight into the barcodes for African diplostomids (Digenea: Diplostomidae): brain parasites in Clarias gariepinus (Siluriformes: Clariidae). Infection, Genetics and Evolution 17, 62–70.CrossRefGoogle ScholarPubMed
Clarke, F., Beeby, A. & Kirby, P. (1989) A study of the macro-invertebrates of Lakes Naivasha, Oloidien and Sonachi, Kenya. Revue d'Hydrobiologie Tropicale 22, 21–33.Google Scholar
Désilets, H.D., Locke, S.A., McLaughlin, J.D. & Marcogliese, D.J. (2013) Community structure of Diplostomum spp. (Digenea: Diplostomidae) in eyes of fish: main determinants and potential interspecific interactions. International Journal for Parasitology 43, 929–939.CrossRefGoogle ScholarPubMed
Flores, V. & Baccala, N. (1998) Multivariate analyses in the taxonomy of two species of Tylodelphys Diesing, 1850 (Trematoda: Diplostomidae) from Galaxias maculatus (Teleostei: Galaxiidae). Sysematic Parasitology 40, 221–227.CrossRefGoogle Scholar
Florio, D., Gustinelli, A., Caffara, M., Turci, F., Quaglio, F., Konecny, R., Nikowitz, T., Wathuta, E.M., Magana, A., Otachi, E.O., Matolla, G.K., Warugu, H.W., Liti, D., Mbaluka, R., Thiga, B., Munguti, J., Akoll, P., Mwanja, W., Asaminew, K. & Tadesse, Z. (2009) Veterinary and public health aspects in tilapia (Oreochromis niloticus niloticus) aquaculture in Kenya, Uganda and Ethiopia [Aspetti veterinari e di sanità pubblica nell'allevamento della tilapia (Oreochromis niloticus niloticus) in Kenya, Uganda ed Etiopia]. Ittiopatologia 6, 51–93.Google Scholar
Galazzo, D.E., Dayanandan, S., Marcogliese, D.J. & McLaughlin, J.D. (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217.CrossRefGoogle Scholar
Gaudet, J.J. & Melack, J.M. (1981) Major ion chemistry in a tropical African lake basin. Journal of Freshwater Biology 11, 309–333.CrossRefGoogle Scholar
Georgieva, S., Soldánová, M., Pérez-del-Olmo, A., Dangel, D.R., Sitko, J., Sures, B. & Kostadinova, A. (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology 43, 57–72.CrossRefGoogle ScholarPubMed
Gherardi, F., Britton, J.R., Mavuthi, K.M., Pacini, N., Grey, J., Tricarico, E. & Harper, D.M. (2011) A review of allodiversity in Lake Naivasha, Kenya: developing conservation actions to protect east African lakes from negative impacts of alien species. Biological Conservation 144, 2585–2596.CrossRefGoogle Scholar
Gibson, D.I. (1996) Trematoda. Part IV. pp. 1–373. in Margolis, L. & Kabata, Z. (Eds) Guide to the parasites of fishes of Canada. Canadian Special Publication of Fisheries and Aquatic Sciences No. 124. Ottawa, NRC Press.Google Scholar
Gichohi, M.C. (2010) Prevalence, intensity and pathological lesions associated with helminth infections in farmed and wild fish in upper Tana River basin, Kenya. PhD thesis, University of Nairobi.Google Scholar
Harper, D.M., Morrison, E.H.J., Macharia, M.M., Mavuthi, K.M. & Upton, C. (2011) Lake Naivasha, Kenya: ecology, society and future. Freshwater Reviews 4, 89–114.CrossRefGoogle Scholar
Hebert, P.D.N., Ratnasingham, S. & deWaard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London series B – Biological sciences 270, S96–S99.Google ScholarPubMed
Hoffman, G.L. & Hundley, J.B. (1957) The life-cycle of Diplostomum baeri eucaliae n. subsp. (Trematoda: Strigeida). Journal of Parasitology 43, 613–627.CrossRefGoogle ScholarPubMed
Hutcheson, G.D. & Sofroniou, N. (1999) The multivariate social scientist: introductory statistics using generalized linear models. London, SAGE Publications.CrossRefGoogle Scholar
Kalbe, M. & Kurtz, J. (2006) Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum. Parasitology 132, 105–116.CrossRefGoogle ScholarPubMed
Karvonen, A., Hudson, P.J., Seppälä, O. & Valtonen, E.T. (2004) Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation. Parasitology Research 92, 183–188.CrossRefGoogle ScholarPubMed
King, P.H. & Van As, J.G. (1997) Description of the adult and larval stages of Tylodelphys xenopi (Trematoda: Diplostomidae) from Southern Africa. Journal of Parasitology 83, 287–295.CrossRefGoogle ScholarPubMed
Locke, S.A., McLaughlin, J.D., Dayanandan, S. & Marcogliese, D.J. (2010a) Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. International Journal for Parasitology 40, 333–343.CrossRefGoogle ScholarPubMed
Locke, S.A., McLaughlin, J.D. & Marcogliese, D.J. (2010b) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827.CrossRefGoogle Scholar
Marcogliese, D.J., Compagna, S., Bergeron, E. & McLaughlin, J.D. (2001a) Population biology of eyeflukes in fish from a large fluvial ecosystem: the importance of gulls and habitat characteristics. Canadian Journal of Zoology 79, 1102–1113.CrossRefGoogle Scholar
Marcogliese, D.J., Dumont, P., Gendron, A.D., Mailhot, Y., Bergeron, E. & McLaughlin, J.D. (2001b) Spatial and temporal variation in the abundance of Diplostomum spp. in walleye (Stizostedion vitreum) and white sucker (Catostomus commersoni) from the St. Lawrence River. Canadian Journal of Zoology 9, 355–369.CrossRefGoogle Scholar
McKeown, C.A. & Irwin, S.W.B. (1995) The life cycle stages of three Diplostomum species maintained in the laboratory. International Journal for Parasitology 25, 897–906.CrossRefGoogle ScholarPubMed
Migiro, K.E., Matolla, G.K., Ouko, V.O. & Victor, N.M. (2012) Diplostomum parasites affecting Oreochromis niloticus in Chepkoilel fish farm and two dams in Eldoret – Kenya. International Journal of Science Engineering Research 3, 1–7.Google Scholar
Morozińska-Gogol, J. (2007) Experimental infection of the black-headed gull Larus ridibundus (L.) with eye-fluke parasites of the three-spined stickleback Gasterosteus aculeatus (L.). Baltic Coastal Zone 11, 59–64.Google Scholar
Moszczynska, A., Locke, S.A., McLaughlin, J.D., Marcogliese, D.J. & Crease, T.J. (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 75–82.CrossRefGoogle ScholarPubMed
Musiba, M.J. & Nkwengulila, G. (2006) Occurrence of metacercariae of Diplostomum and Tylodelphys species (Diplostomidae) in Clarias species (Clariidae) from Lake Victoria. Tanzania Journal of Science 32, 89–98.Google Scholar
Mutia, G.M., Ntiba, M.J., Mavuti, K.M. & Omondi, G. (2010) Some observations on the spawning season of Barbus amphigramma in Lake Naivasha, Kenya. Aquatic Ecosystem Health and Management 13, 214–221.CrossRefGoogle Scholar
Mwita, C.J. & Nkwengulila, G. (2010) Phylogenetic relationships of the metazoan parasites of the clariid fishes of Lake Victoria inferred from partial 18S rDNA sequences. Tanzania Journal of Science 36, 47–57.Google Scholar
Niewiadomska, K. (1996) The genus Diplostomum – taxonomy, morphology and biology. Acta Parasitologica 41, 55–56.Google Scholar
Niewiadomska, K. & Laskowski, Z. (2002) Systematic relationships among six species of Diplostomum Nordmann, 1832 (Digenea) based on morphological and molecular data. Acta Parasitologica 47, 1230–1237.Google Scholar
Niewiadomska, K. & Niewiadomska-Bugaj, M. (1995) Optimal identification procedure for Diplostomum paracaudum (Iles, 1959) and D. pseudospathaceum Niewiadomska, 1984 metacercariae (Digenea) based on morphological characters. Systematic Parasitology 30, 165–171.CrossRefGoogle Scholar
Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Littlewood, D.T.J. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle ScholarPubMed
Osborne, J.W. & Costello, A.B. (2004) Sample size and subject to item ratio in principal components analysis. Practical Assessment, Research and Evaluation 9. Available athttp://www.pareonline.net/getvn.asp?v = 9n = 11 (accessed accessed 12 September 2013).Google Scholar
Otachi, E.O. (2009) Studies on occurrence of protozoan and helminth parasites in Nile Tilapia (Oreochromis niloticus L.) from central and eastern provinces, Kenya. MSc Thesis, Egerton University, Kenya.Google Scholar
Otachi, E., Wathuta, E., Magana, A., Fioravanti, M.-L., Florio, D. & Konecny, R. (2011) Comparative ecological analysis of fish parasitofauna in a hub-plot aquaculture system: implications for aquaculture in Kenya. Egerton Journal of Science and Technology 11, 87–103.Google Scholar
Otachi, E., Magana, A.M., Jirsa, F. & Fellner-Frank, C. (2014) Parasites of commercially important fish from Lake Naivasha, Rift Valley, Kenya. Parasitology Research 113, 1057–1067.CrossRefGoogle ScholarPubMed
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. Molecular Phylogenetics and Evolution 48, 369–371.CrossRefGoogle Scholar
Poulin, R. & Mouillot, D. (2005) Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511–514.CrossRefGoogle ScholarPubMed
Rauch, G., Kalbe, M. & Reusch, T.B.H. (2005) How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 1069–1075.CrossRefGoogle ScholarPubMed
Rellstab, C., Louhi, K.-R., Karvonen, A. & Jokela, J. (2011) Analysis of trematode parasite communities in fish eye lenses by pyrosequencing of naturally pooled DNA. Infection, Genetics and Evolution 11, 1276–1286.CrossRefGoogle ScholarPubMed
Rousseeuw, P.J. (1987) Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. Journal of Computational and Applied Mathematics 20, 53–65.CrossRefGoogle Scholar
Schäperclaus, W. (1990) Fischkrankheiten. Berlin, Akademie Verlag.Google Scholar
Sereno-Uribe, A.L., Pinacho-Pinacho, C.D., García-Varela, M. & 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.CrossRefGoogle ScholarPubMed
Styczynska-Jurewicz, E. (1959) Expansion of cercariae of Diplostomum spathaceum Rud. 1819, a common parasite of fishes, in the littoral zone of the lake. Polskie Arch-iwum Hydrobiologii 6, 105–116.Google Scholar
Sweeting, R.A. (1974) Investigations into natural and experimental infections of freshwater fish by the common eye-fluke Diplostomum spathaceum Rud. Parasitology 69, 291–300.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Valtonen, E.T. & Gibson, D.I. (1997) Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities of northern Finland. Annals Zoologici Fennici 34, 47–59.Google Scholar
Welcomme, R.L. (1979) Fisheries ecology of floodplain rivers. London, Longman.Google Scholar