Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-25T09:26:45.717Z Has data issue: false hasContentIssue false

Parasite identification, succession and infection pathways in perch fry (Perca fluviatilis): new insights through a combined morphological and genetic approach

Published online by Cambridge University Press:  02 January 2013

JASMINCA BEHRMANN-GODEL*
Affiliation:
Limnological Institute, University of Konstanz, 78464 Konstanz, Germany
*
*Corresponding author: Tel: + + 49 7531 884536. Fax: + + 49 7531 883533. E-mail:[email protected]

Summary

Identification of parasite species is particularly challenging in larval and juvenile hosts, and this hampers the understanding of parasite acquisition in early life. The work described here employs a new combination of methods to identify parasite species and study parasite succession in fry of perch (Perca fluviatilis) from Lake Constance, Germany. Classical morphological diagnostics are combined with sequence comparisons between parasite life-stages collected from various hosts within the same ecosystem. In perch fry at different stages of development, 13 different parasite species were found. Incomplete morphological identifications of cestodes of the order Proteocephalidea, and trematodes of the family Diplostomatidae were complemented with sequences of mitochondrial DNA (cytochrome oxidase 1) and/or nuclear (28 s rDNA) genes. Sequences were compared to published data and used to link the parasites in perch to stages from molluscs, arthropods and more easily identifiable developmental stages from other fishes collected in Lake Constance, which both aided parasite identification and clarified transmission pathways. There were distinct changes in parasite community composition and abundance associated with perch fry age and habitat shifts. Some parasites became more abundant in older fish, whereas the composition of parasite communities was more strongly affected by the ontogenetic shifts from the pelagic to the littoral zone.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013

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

REFERENCES

Andersen, K. (1978). The helminths in the gut of perch (Perca fluviatilis L.) in a small oligotrophic lake in southern Norway. Zeitschrift für Parasitenkunde 56, 1727.CrossRefGoogle Scholar
Andrews, C. (1979). Host specificity of the parasite fauna of perch Perca fluviatilis L. from the British Isles, with special reference to a study at Llyn Tegid (Wales). Journal of Fish Biology 15, 195209.CrossRefGoogle Scholar
Balbuena, J. A., Karlsbakk, E., Kvenseth, A. M., Saksvik, M. and Nylund, A. (2000). Growth and emigration of third-stage larvae of Hysterothylacium aduncum (nematoda: anisakidae) in larval herring Culpea harengus. Journal of Parasitology 86, 12711275.CrossRefGoogle Scholar
Balling, T. E. and Pfeiffer, W. (1997 a). Frequency distribution of fish parasites in the perch Perca fluviatilis L. from Lake Constance. Parasitology Research 83, 370373.CrossRefGoogle ScholarPubMed
Balling, T. E. and Pfeiffer, W. (1997 b). The parasitism of fish from Lake Constance: A comparison of present and earlier data. Parasitology Research 83, 793796.CrossRefGoogle Scholar
Balling, T. E. and Pfeiffer, W. (1997 c). Seasonal differences in infestation of the perch Perca fluviatilis L. from Lake Constance with digenean trematodes. Parasitology Research 83, 789792.CrossRefGoogle ScholarPubMed
Balling, T. E. and Pfeiffer, W. (1997 d). Location-dependent infection of fish parasites in Lake Constance. Journal of Fish Biology 51, 10251032.Google Scholar
Bertrand, M., Marcogliese, D. J. and Magnan, P. (2008). Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. Journal of Fish Biology 72, 555572.CrossRefGoogle Scholar
Bykhovskaya-Pavlovskaya, I., Gusev, A., Dubinina, M., Izyumova, N., Smirnova, T., Sokolovskaya, I., Shtein, G., Shul´man, S. and Epshtein, V. (1964). Key to Parasites of Freshwater Fish of the U.S.S.R. Akademiya Nauk SSSR.Google Scholar
Campana, S. E. (1992). Measurement and interpretation of the microstructure of fish otoliths. In Otolith Microstructure, Examination and Analysis (ed. Stevenson, K. D. and Campana, S. E.). Canadian Special Publication of Fisheries and Aquatic Sciences. 117, pp. 5971.Google Scholar
Carney, J. P., and Dick, T. A. (1999). Enteric helminths of perch (Perca fluviatilis L.) and yellow perch (Perca flavescens Mitchill): stochastic or predictable assemblages? Journal of Parasitology 85, 785795.CrossRefGoogle ScholarPubMed
Clarke, K. R. (1993). Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117143.CrossRefGoogle Scholar
Coles, T. (1981). The distribution of perch, Perca fluviatilis L. throughout their first year of life in Llyn Tegid, North Wales. Archiv für Fischereiwissenschaft 15, 193204.Google Scholar
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198202.Google ScholarPubMed
Eckmann, R. and Imbrock, F. (1996). Distribution and diel vertical migration of Eurasian perch (Perca fluviatilis L.) during winter. Annales Zoologici Fennici 33, 679686.Google Scholar
Faltýnková, A. (2005). Laval trematodes (Digenea) in molluscs from small water bodies near Ceske Budejovice, Czech Republic. Acta Parasitologica 50, 4955.Google Scholar
Faltýnková, A., Karvonen, A., Jyrkkä, M. and Valtonen, E. T. (2009). Being successful in the world of narrow opportunities: transmission patterns of the trematode Ichthyocotylurus pileatus. Parasitology 136, 13751382.CrossRefGoogle ScholarPubMed
Galazzo, D. E., Dayanandan, S., Marcogliese, D. J. and 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, 22072217.CrossRefGoogle Scholar
Grutter, A. S., Cribb, T. H., McCallum, H., Pickering, J. L. and McCormick, M. I. (2009). Effects of parasites on larval and juvenile stages of the coral reef fish Pomacentrus moluccensis. Coral Reefs 29, 3140.CrossRefGoogle Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium 41, 9598.Google Scholar
Hanzelová, V., Scholz, T., Gerdeaux, D. and Kuchta, R. (2002). A comparative study of Eubothrium salvelini and E. crassum (Cestoda: Pseudophyllidea) parasites of arctic charr and brown trout in Alpine lakes. Environmental Biology of Fishes 64, 245256.CrossRefGoogle Scholar
Imbrock, F., Appenzeller, A. and Eckmann, R. (1996). Diel and seasonal distribution of perch in Lake Constance: a hydroacoustic study and in situ observations. Journal of Fish Biology 49, 113.Google Scholar
Johnson, M. W., Nelson, P. A. and Dick, T. A. (2004). Structuring mechanisms of yellow perch (Perca flavescens) parasite communities: host age, diet, and local factors. Canadian Journal of Zoology 82, 12911301.CrossRefGoogle Scholar
Johnson, P. T. J., Stanton, D. E., Preu, E. R., Forshay, K. J. and Carpenter, S. R. (2006). Dining on disease: How interactions between infection and Environment affect predation risk. Ecology 87, 19731980.CrossRefGoogle ScholarPubMed
Kelly, D. W., Thomas, H., Thieltges, D. W., Poulin, R. and Tompkins, D. M. (2010). Trematode infection causes malformations and population effects in a declining New Zealand fish. Journal of Animal Ecology 79, 445452.CrossRefGoogle Scholar
Kennedy, C. R. (1978). The biology, specificity and habitat of the species of Eubothrium (Cestoda: Pseudophyllidea), with reference to their use as biological tags: a review. Journal of Fish Biology 12, 393410.CrossRefGoogle Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.CrossRefGoogle ScholarPubMed
King, S. D. and Cone, D. K. (2009). Infections of Dactylogyrus pectenatus (Monogenea: Dactylogyridae) on Larvae of Pimephales promelas (Teleostei: Cyprinidae) in Scott Lake, Ontario, Canada. Comparative Parasitology 76, 110112.CrossRefGoogle Scholar
Kruskal, J. B. (1964). Nonmetric multidimensional scaling: A numerical method. Psychometrika 29, 115129.CrossRefGoogle Scholar
Kuchta, R., Cech, M., Scholz, T., Soldanova, M., Levron, C. and Skorikova, B. (2009). Endoparasites of European perch Perca fluviatilis fry: role of spatial segregation. Diseases of Aquatic Organisms 86, 8791.CrossRefGoogle ScholarPubMed
Kuperman, B. I. (1981). Tapeworms of the genus Triaenophorus, Parasites of Fishes. Amerind Publishing, New York, USA.Google Scholar
Lahnsteiner, F., Kletzl, M. and Weismann, T. (2009). The risk of parasite transfer to juvenile fishes by live copepod food with the example Triaenophorus crassus and Triaenophorus nodulosus. Aquaculture 295, 120125.CrossRefGoogle Scholar
Locke, S. A., Daniel McLaughlin, J. and Marcogliese, D. J. (2010 a). 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, 28132827.CrossRefGoogle Scholar
Locke, S. A., McLaughlin, J. D., Dayanandan, S. and Marcogliese, D. J. (2010 b). 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, 333343.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. (1995). The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5, 336371.CrossRefGoogle Scholar
McCairns, R. J. S. and Fox, M. G. (2004). Habitat and home range fidelity in a trophically dimorphic pumpkinseed sunfish (Lepomis gibbosus) population. Oecologia, 140, 271279.CrossRefGoogle Scholar
Miehls, S. M. and Dettmers, J. M. (2011). Factors Influencing Habitat Shifts of Age-0 Yellow Perch in Southwestern Lake Michigan. Transactions of the American Fisheries Society 140, 13171329.CrossRefGoogle Scholar
Morozinska-Gogol, J. (2008). A check-list of parasites of percid fishes (Actinopterygii: Percidae) from the estuaries of the Polish coastal zone. Helminthologia 45, 196203.CrossRefGoogle Scholar
Moszczynska, A., Locke, S. A., McLaughlin, J. D., Marcogliese, D. J. and 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.CrossRefGoogle ScholarPubMed
Nendick, L., Sackville, M., Tang, S., Brauner, C. J. and Farrell, A. P. (2011). Sea lice infection of juvenile pink salmon (Oncorhynchus gorbuscha): effects on swimming performance and postexercise ion balance. Canadian Journal of Fisheries and Aquatic Sciences 68, 241249.CrossRefGoogle Scholar
Niewiadomska, K. and Szymanski, S. (1991). Host-induced variability of Diplostomum paracaudum (Iles, 1959) metacercariae (Digenea). Acta Parasitolgica Warszawa 36, 1117.Google Scholar
Niewiadomska, K. and Kiseliene, V. (1994). Diplostomum cercariae (Digenea) in snails from Lithuania. II. Survey of species. Acta Parasitolgica Warszawa 39, 179186.Google Scholar
Niewiadomska, K. and Laskowski, Z. (2002). Systematic relationships among six species of Diplostomum Nordmann, 1832 (Digenea) based on morphological and molecular data. Acta Parasitolgica Warszawa 47, 2028.Google Scholar
Olson, P. D., Littlewood, D. T., Bray, R. A. and Mariaux, J. (2001). Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 19, 443467.CrossRefGoogle ScholarPubMed
Pracheil, B. M. and Muzzall, P. M. (2009). Chronology and development of juvenile bluegill parasite communities. Journal of Parasitology 95, 838845.CrossRefGoogle ScholarPubMed
Pronin, N. M. (1990). Structure of the cestode population of Triaenophorus nodulosus (Pseudophyllidea, Triaenophoridae) in the ecosystem of Lake Shchuchic and the mortality of the helminth at various stages of development. Ekologija. Lietuvos Mokslu Akademija Vilnius 3, 4855.Google Scholar
Reckel, F., Melzer, R. R. and Smola, U. (1999). Ultrastructure of the retina of two subspecies of Coregonus lavaretus (Teleostei) from Lake Constance (Germany). Acta Zoolgica 80, 153162.CrossRefGoogle Scholar
Rosenthal, H. (1967). Parasites in larvae of the herring (Clupea harengus L.) fed with wild plankton. Marine Biology 1, 1015.CrossRefGoogle Scholar
Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406425.Google Scholar
Schäperclaus, W. (1979). Fischkrankheiten. Vol 4. Akademie-Verlag, Berlin, Germany.Google Scholar
Scholz, T., Drabek, R. and Hanzelova, V. (1998). Scolex morphology of Proteocephalus tapeworms (Cestoda: Proteocephalidae), parasites of freshwater fish in the Palaearctic Region. Folia Parasitologica Praha 45, 2743.Google ScholarPubMed
Scholz, T. (1999). Life cycle of species of Proteocephalus, parasites of fishes in the Palearctic Region: a review. Journal of Helmithology 73, 119.CrossRefGoogle ScholarPubMed
Scholz, T., Hanzelova, V., Skerikova, A., Shimazu, T. and Rolbiecki, L. (2007). An annotated list of species of the Proteocephalus Weinland, 1858 aggregate sensu de Chambrier et al. (2004) (Cestoda: Proteocephalidea), parasites of fishes in the Palaearctic Region, their phylogenetic relationships and a key to their identification. Systematic Parasitology 67, 139156.CrossRefGoogle Scholar
Secombes, C. J. and Chappell, L. H. (1996). Fish immune responses to experimental and natural infection with helminth parasites. Annual Review of Fish Diseases 6, 167177.CrossRefGoogle Scholar
Skovgaard, A., Bahlool, Q. Z. M., Munk, P., Berge, T. and Buchmann, K. (2009 a). Infection of North Sea cod, Gadus morhua L., larvae with the parasitic nematode Hysterothylacium aduncum Rudolphi. Journal of Plankton Research 33, 13111316.CrossRefGoogle Scholar
Skovgaard, A., Meneses, I. and Angélico, M. M. (2009 b). Identifying the lethal fish egg parasite Ichthyodinium chabelardi as a member of Marine Alveolate Group I. Environmental Microbiology 11, 20302041.CrossRefGoogle ScholarPubMed
Sonnenberg, R., Nolte, A. W. and Tautz, D. (2007). An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Frontiers in Zoology 4, 6.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.CrossRefGoogle ScholarPubMed
Valtonen, E. T., Holmes, J. C., Aronen, J. and Rautalahti, I. (2003). Parasite communities as indicators of recovery from pollution: parasites of roach (Rutilus rutilus) and perch (Perca fuviatilis) in central Finland. Parasitology 126 (Suppl), S43S52.CrossRefGoogle Scholar
Vojtek, J. (1989). The present situation of the research into the stages of development of trematodes in Czechoslovakia. Scripta Facultatis Scientiarum Naturalium Universitatis Prukynianae Brunensis. Brno 19, 339352.Google Scholar
Wang, N. and Eckmann, R. (1994). Distribution of perch (Perca fluviatilis L.) during their first year of life in Lake Constance. Hydrobiologia 277, 135143.CrossRefGoogle Scholar
Wang, N. and Appenzeller, A. (1998). Abundance, depth distribution, diet composition and growth of perch (Perca fluviatilis) and burbot (Lota lota) larvae and juveniles in the pelagic zone of Lake Constance. Ecology of Freshwater Fish 7, 176183.CrossRefGoogle Scholar
Weber, M. J., Dettmers, J. M. and Wahl, D. H. (2011). Growth and survival of age-0 yellow perch across habitats in southwestern Lake Michigan: early life history in a large freshwater environment. Transactions of the American Fisheries Society 140, 1172.CrossRefGoogle Scholar
Wootten, R. (1974). Studies on the life history and development of Proteocephalus percae (Müller) (Cestoda: Proteocephalidea). Journal of Helmithology 48, 269281.CrossRefGoogle ScholarPubMed
Wootton, J. R. (1998). Ecology of Teleost Fishes, 2nd Edn.Chapman and Hall, New York, USA.Google Scholar
Zehnder, M. P. and Mariaux, J. (1999). Molecular systematic analysis of the order Proteocephalidea (Eucestoda) based on mitochondrial and nuclear rDNA sequences. International Journal for Parasitology 29, 18411852.CrossRefGoogle ScholarPubMed
Zelmer, D. A. and Arai, H. P. (2004). Development of nestedness: host biology as a community process in parasite infracommunities of yellow perch (Perca flavescens (Mitchill)) from Garner Lake, Alberta. Journal of Parasitology 90, 435436.CrossRefGoogle ScholarPubMed
Supplementary material: File

Behrmann-Godel Supplementary Material

Appendix

Download Behrmann-Godel Supplementary Material(File)
File 11.6 MB