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The distribution of digenean metacercariae within bream (Abramis brama) gill apparatus: preferences, co-occurrence and interactions of parasites

Published online by Cambridge University Press:  24 May 2017

M. Zolovs*
Affiliation:
Institute of Life Sciences and Technology, Daugavpils University, Parādes Street 1a, Daugavpils, Latvia, LV5401
J. Kanto
Affiliation:
Institute of Life Sciences and Technology, Daugavpils University, Parādes Street 1a, Daugavpils, Latvia, LV5401
I. Jakubāne
Affiliation:
Institute of Life Sciences and Technology, Daugavpils University, Parādes Street 1a, Daugavpils, Latvia, LV5401
*
*E-mail address: [email protected]

Abstract

Species-specific microenvironmental preferences and interactions between parasite species have been the focus of many ecological studies. Here, we studied the distribution of ectoparasite species within the gill apparatus of bream (Abramis brama) from Lake Lubāns (Latvia) to establish whether digenean metacercariae: (1) prefer specific patches within the gill apparatus; (2) co-occur in the same patches with monogeneans and copepods within a host individual; and (3) interact with monogeneans and copepods. We recorded all parasites on gill arches of the same host species and used null models to analyse co-occurrences of digenean metacercariae, monogeneans and copepods. Zero-inflated mixture models were used to define the preferred patches of parasites. We found that digenean metacercariae (Bucephalus polymorphus) prefer specific patches of the gill apparatus to encyst, and shared these preferences with monogeneans and copepods, but did not interact with them. We concluded that digenean metacercariae have a species-specific microenvironmental preference to encyst in the gill apparatus and their occurrence (even in high numbers) does not reduce the success of attachment of monogeneans and copepods in the same gill patches.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2017 

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References

Alvarez-Pellitero, P. (2008) Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Veterinary Immunology and Immunopathology 126, 171198.CrossRefGoogle ScholarPubMed
Barnard, K., Krasnov, B., Goff, L. & Matthee, S. (2015) Infracommunity dynamics of chiggers (Trombiculidae) parasitic on a rodent. Parasitology 142, 16051611.CrossRefGoogle ScholarPubMed
Bauer, O.N. (1987) Identification key to parasites of freshwater fish USSR. 583 pp. Leningrad, Nauka.Google Scholar
Blažek, R. & Gelnar, M. (2006) Temporal and spatial distribution of glochidial larval stages of European unionid mussels (Mollusca: Unionidae) on host fishes. Folia Parasitologica 53, 98106.CrossRefGoogle ScholarPubMed
Blazer, V.S. & Gratzek, J.B. (1985) Cartilage proliferation in response to metacercarial infections of fish gills. Journal of Comparative Pathology 95, 273280.CrossRefGoogle ScholarPubMed
Bogéa, T. & Caira, J.N. (2001) Ultrastructure and chaetotaxy of sensory receptors in the cercariae of a species of Crepidostomum Braun, 1900 and Bunodera Railliet, 1896 (Digenea: Allocreadiidae). Journal of Parasitology 87, 273286.CrossRefGoogle ScholarPubMed
Buchmann, K. (1988) Spatial distribution of Pseudodactylogyrus anguillae and P. bini (Monogenea) on the gills of the European eel, Anguilla anguilla. Journal of Fish Biology 32, 801802.CrossRefGoogle Scholar
Buchmann, K. (1989) Relationship between host size of Anguilla anguilla and the infection level of the monogeneans Pseudodactylogyrus spp. Journal of Fish Biology 35, 599601.CrossRefGoogle Scholar
Buchmann, K. & Bresciani, J. (1998) Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: association between mucous cell density in skin and site selection. Parasitology Research 84, 1724.CrossRefGoogle ScholarPubMed
Buchmann, K. & Lindenstrøm, T. (2002) Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology 32, 309319.CrossRefGoogle ScholarPubMed
Dmitrieva, E. (2000) Distribution of the Black Sea monogeneans on fish gills. Inter- and intraspecific relationships as cause of their distribution. Ekologiya Morya 53, 3640.Google Scholar
Dobson, A.P. (1988) The population biology of parasiteinduced changes in host behavior. The Quarterly Review of Biology 63, 139165.CrossRefGoogle ScholarPubMed
Dzika, E. (1999) Microhabitats of Pseudodactylogyrus anguillae and P. bini (Monogenea: Dactylogyridae) on the gills of large-size European eel Anguilla anguilla from Lake Gaj, Poland. Folia Parasitologica 46, 3336.Google Scholar
Dzika, E. (2002) The parasites of bream Abramis brama (L.) from Lake Kortowskie. Archives of Polish Fisheries 10, 8596.Google Scholar
Dzika, E., Kuształa, M. & Kazłowski, J. (2008) Metazoan parasite fauna of fish species from Lake Kortowskie. Archives of Polish Fisheries 16, 7586.CrossRefGoogle Scholar
El Hafidi, F., Berrada-Rkhami, O., Benazzou, T. & Gabrion, C. (1998) Microhabitat distribution and coexistence of Microcotylidae (Monogenea) on the gills of the striped mullet Mugil cephalus: chance or competition? Parasitology Research 84, 315320.CrossRefGoogle ScholarPubMed
Entsminger, G.L. (2014) EcoSim professional: Null modeling software for ecologists, Version 1. Montrose, Colorado, Acquired Intelligence Inc., Kesey-Bear and Pinyon Publishing. Available at http://www.garyentsminger.com/ecosim/index.htm (accessed 10 March 2017).Google Scholar
Friggens, M.M. & Brown, J.H. (2005) Niche partitioning in the cestode communities of two elasmobranchs. Oikos 108, 7684.CrossRefGoogle Scholar
Galaktionov, K.V. & Dobrovolskij, A.A. (1998) The origin and evolution of trematode life cycles. 404 pp. Saint Petersburg, Nauka.Google Scholar
Gotelli, N.J. (2000) Null model analysis of species co-occurrence patterns. Ecology 81, 26062621.CrossRefGoogle Scholar
Gotelli, N.J. & McCabe, D.J. (2002) Species co-occurrence: a meta-analysis of J.M. Diamond's assembly rules model. Ecology 83, 20912096.CrossRefGoogle Scholar
Gotelli, N.J. & Ulrich, W. (2010) The empirical Bayes approach as a tool to identify non-random species associations. Oecologia 162, 463477.CrossRefGoogle ScholarPubMed
Grabe, K. & Haas, W. (2004) Navigation within host tissues: Schistosoma mansoni and Trichobilharzia ocellata schistosomula respond to chemical gradients. International Journal for Parasitology 34, 927934.CrossRefGoogle ScholarPubMed
Gussev, A.V. (1985) Identification key to parasites of freshwater fish of USSR. 424 pp. Leningrad, Nauka.Google Scholar
Gutierrez, P.A. & Martorelli, S.R. (1999) Niche preferences and spatial distribution of Monogenea on the gills of Pimelodus maculatus in Río de la Plata (Argentina). Parasitology 119, 183188.CrossRefGoogle Scholar
Haas, W. (1994) Physiological analysis of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109, S15S29.CrossRefGoogle Scholar
Haas, W. (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology (Jena) 106, 349364.CrossRefGoogle ScholarPubMed
Haas, W., Granzer, M. & Brockelman, C.R. (1990) Opisthorchis viverrini: finding and recognition of the fish host by the cercariae. Experimental Parasitology 71, 422431.CrossRefGoogle ScholarPubMed
Hoar, W.S. & Randall, D.J. (1984) Fish physiology. Part A: Anatomy, gas transfer, and acid–base regulation. 456 pp. Orlando, Florida, Academic Press.Google Scholar
Holmes, J.C. & Price, P.W. (1986) Communities of parasites. pp. 187213 in Kikkawa, J. & Anderson, D.J. (Eds) Community ecology: Patterns and processes. Oxford, Blackwell Scientific Publications.Google Scholar
Ives, A. (1988) Aggregation and the coexistence of competitors. Annales Zoologici Fennici 25, 7588.Google Scholar
Jackman, S. (2015) pscl: classes and methods for R developed in the political science computational laboratory, Stanford University. Department of Political Science, Stanford University, Stanford, California. R package version 1.4.9. Available at http://pscl.stanford.edu/ (accessed 10 March 2017).Google Scholar
Johnson, P.T., Lunde, K.B., Ritchie, E.G. & Launer, A.E. (1999) The effect of trematode infection on amphibian limb development and survivorship. Science 284, 802804.CrossRefGoogle ScholarPubMed
Kemp, W.M. & Devine, D.P. (1982) Behavioral cues in trematode life cycles. Cues that influence behavior of internal parasites. Proceedings of a Workshop, Auburn, Alabama United States, 21–23 September 1981, pp. 67–84.Google Scholar
Koskivaara, M. & Valtonen, E. (1992) Dactylogyrus (Monogenea) communities on the gills of roach in the lakes in Central Finland. Parasitology 104, 263272.CrossRefGoogle Scholar
Koskivaara, M., Valtonen, E.T. & Vuori, K.M. (2009). Microhabitat distribution and coexistence of Dactylogyrus species (Monogenea) on the gills of roach. Parasitology 104, 273281.CrossRefGoogle Scholar
Krasnov, B., Vinarski, M., Korallo-Vinarskaya, N.P., Mouillot, D. & Poulin, R. (2009) Inferring associations among parasitic gamasid mites from census data. Oecologia 160, 175185.CrossRefGoogle ScholarPubMed
Krebs, C.J. (1998) Ecological methodology. pp. 597653. New York, Addison–Welsey Education Publishers.Google Scholar
Krejci, K.G. & Fried, B. (1994) Light and scanning electron microscopic observations of eggs, daughter rediae, cercariae, and encysted metacercariae of Echinostoma trivolvis and E. caproni. Parasitology Research 80, 4247.CrossRefGoogle ScholarPubMed
Llewellyn, J. (1956) The host-specificity, micro-ecology, adhesive attitudes, and comparative morphology of some trematode gill parasites. Journal of the Marine Biological Association of the United Kingdom 35, 113127.CrossRefGoogle Scholar
Martin, T.G., Wintle, B.A., Rhodes, J.R., Kuhnert, P.M., Field, S.A., Low-Choy, S.J., Tyre, A.J. & Possingham, H.P. (2005) Zero tolerance ecology: improving ecological inference by modelling the source of zero observations. Ecology Letters 8, 12351246.CrossRefGoogle ScholarPubMed
Matejusová, I., Simková, A., Sasal, P. & Gelnar, M. (2003) Microhabitat distribution of Pseudodactylogyrus anguillae and Pseudodactylogyrus bini among and within gill arches of the European eel (Anguilla anguilla L.). Parasitology Research 89, 290296.CrossRefGoogle ScholarPubMed
Mitchell, A.J., Salmon, M.J., Huffman, D.G., Goodwin, A.E. & Brandt, T.M. (2000) Prevalence and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish, the fountain darter, in two central Texas spring-fed rivers. Journal of Aquatic Animal Health 12, 283289.2.0.CO;2>CrossRefGoogle Scholar
Morand, S., Poulin, R., Rohde, K. & Hayward, C. (1999) Aggregation and species coexistence of ectoparasites of marine fishes. International Journal for Parasitology 29, 663672.CrossRefGoogle ScholarPubMed
Olson, K.R. (2002) Vascular anatomy of the fish gill. Journal of Experimental Zoology 293, 214231.CrossRefGoogle ScholarPubMed
Olson, R.E. & Pierce, J.R. (1997) A trematode metacercaria causing gill cartilage proliferation in steelhead trout from Oregon. Journal of Wildlife Diseases 33, 886890.CrossRefGoogle ScholarPubMed
Ostrowski De Nuñez, M. & Haas, W. (2009) Penetration stimuli of fish skin for Acanthostomum brauni cercariae. Parasitology 102, 101104.CrossRefGoogle Scholar
Ottová, E., Šimková, A., Jurajda, P., Dávidová, M., Ondračková, M., Pečínková, M. & Gelnar, M. (2005) Sexual ornamentation and parasite infection in males of common bream (Abramis brama): a reflection of immunocompetence status or simple cost of reproduction? Evolutionary Ecology Research 7, 581593.Google Scholar
Pariselle, A. & Matricon-gondran, M. (1985) A new type of ciliated sensory receptor in the cercariae of Nicolla gallica (Trematoda). Parasitenkude 71, 353364.CrossRefGoogle Scholar
Pianka, E.R. (1974) Niche overlap and diffuse competition. Proceedings of the National Academy of Sciences, USA 71, 21412145.CrossRefGoogle ScholarPubMed
Pilosof, S., Lareschi, M. & Krasnov, B. (2012) Host body microcosm and ectoparasite infracommunities: arthropod ectoparasites are not spatially segregated. Parasitology 139, 17391748.CrossRefGoogle Scholar
Pronkina, N.V., Dmitrieva, E.V. & Gerasev, P.I. (2010) Distribution of two species of genus Ligophorus Euzet et Suriano, 1977 (Plathelmintes: Monogenea) on gills of Liza aurata (Risso, 1810) (Pisces: Mugilidae) from the Black Sea. Morsky Ekologichny Journal 9, 5362.Google Scholar
R Development Core Team (2016) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at http://www.R-project.org (accessed 17 May 2017).Google Scholar
Ridout, M., Demétrio, C.G.B. & Hinde, J. (1998) Models for count data with many zeros. Proceedings of the International Biometric Conference, Cape Town, December 1998, pp. 1–13.Google Scholar
Rodrigues, A.A. & Saraiva, A. (1996) Spatial distribution and seasonality of Pseudodactylogyrus anguillae and P. bini (Monogenea: Pseudodactylogyridae) on the gills of the European eel Anguilla anguilla from Portugal. Bulletin of the European Association of Fish Pathologists 16, 8588.Google Scholar
Rohde, K. (1977) Habitat partitioning in monogenea of marine fishes. Zeitschrift für Parasitenkunde 53, 171182.CrossRefGoogle Scholar
Rohde, K. (1979) A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114, 648671.CrossRefGoogle Scholar
Rohde, K. (1991) Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos 60, 91104.CrossRefGoogle Scholar
Rohde, K. (2002) Niche restriction and mate finding in vertebrate hosts. pp. 171197 in Lewis, E.E., Campbell, J.F. & Sukhdeo, M.V.K. (Eds) The behavioural ecology of parasites. London, UK, CAB International.CrossRefGoogle Scholar
Rohde, K. (2013) The balance of nature and human impact. 426 pp. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Rückert, S., Klimpel, S. & Palm, H. (2007) Parasite fauna of bream Abramis brama and roach Rutilus rutilus from a man-made waterway and a freshwater habitat in northern Germany. Diseases of Aquatic Organisms 74, 225233.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. & Valtonen, T. (2004) Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Animal Behaviour 68, 257263.CrossRefGoogle Scholar
Shaw, D.J. & Dobson, A.P. (1995) Patterns of macroparasites abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, 111133.CrossRefGoogle ScholarPubMed
Shoaibi Omrani, B., Ebrahimzadeh Mousavi, H.A. & Sharifpour, I. (2010) Occurrence and histopathology of Ascocotyle tenuicollis metacercaria in gill of platyfish (Xiphophorus maculatus) imported to Iran. Iranian Journal of Fisheries Sciences 9, 472477.Google Scholar
Short, R.B. & Cartrett, M.L. (1973) Argentophilic ‘receptors’ of Schistosoma mansoni cercariae. Journal of Parasitology 59, 10411059.CrossRefGoogle ScholarPubMed
Simková, A., Desdevises, Y., Gelnar, M. & Morand, S. (2000) Co-existence of nine gill ectoparasites (Dactylogyrus: Monogenea) parasitising the roach (Rutilus rutilus L.): History and present ecology. International Journal for Parasitology 30, 10771088.CrossRefGoogle ScholarPubMed
Simková, A., Gelnar, M. & Sasal, P. (2001) Aggregation of congeneric parasites (Monogenea: Dactylogyrus) among gill microhabitats within one host species (Rutilus rutilus L.). Parasitology 123, 599607.CrossRefGoogle ScholarPubMed
Soylu, E., Çolak, S.O., Erdogan, F., Erdogan, M. & Tektas, N. (2013) Microhabitat distribution of Pseudodactylogyrus anguillae (Monogenea), Ergasilus gibbus and Ergasilus lizae (Copepoda) on the gills of European eels (Anguilla anguilla, L.). Acta Zoologica Bulgarica 65, 251257.Google Scholar
Stone, L. & Roberts, A. (1990) The checkerboard score and species distributions. Oecologia 85, 7479.CrossRefGoogle ScholarPubMed
Sukhdeo, M.V.K. (1990) Habitat selection by helminths: a hypothesis. Parasitology Today 6, 234237.CrossRefGoogle ScholarPubMed
Sukhdeo, M.V.K. & Mettrick, D.F. (1987) Parasite behaviour: understanding platyhelminth responses. Advances in Parasitology 26, 73144.CrossRefGoogle ScholarPubMed
Sukhdeo, M., Sukhdeo, S.C. & Mettrick, D.F. (1987) Site-finding behaviour of Fasciola hepatica (Trematoda), a parasitic flatworm. Behaviour 103, 174186.CrossRefGoogle Scholar
Sulman, S.S. (1984) Identification key to parasites of freshwater fish of USSR. 428 pp. Leningrad, Nauka.Google Scholar
Sutherland, D.R. & Wittrock, D.D. (1985) The effects of Salmincola californiensis (Copepoda: Lernaeopodidae) on the gills of farm-raised rainbow trout, Salmo gairdneri. Canadian Journal of Zoology 63, 28932901.CrossRefGoogle Scholar
Ulrich, W. (2008) Pairs – a FORTRAN program for studying pair wise species associations in ecological matrices. Torun, Poland. Available at ftp://raksti.daba.lv/pub/GIS/datu_analiize/UlrichW/PairsManual.pdf (accessed 10 March 2017).Google Scholar
Wilson, J.M. & Laurent, P. (2002) Fish gill morphology: inside out. Journal of Experimental Zoology 293, 192213.CrossRefGoogle ScholarPubMed
Woo, P. & Buchmann, K. (2012) Fish parasites: Pathobiology and protection. 383 pp. London, UK, CAB International.CrossRefGoogle Scholar
Wootten, R. (1974) The spatial distribution of Dactylogyrus amphibothrium on the gills of ruffe Gymnocephalus cernua and its relation to the relative amounts of water passing over the parts of the gills. Journal of Helminthology 48, 167174.CrossRefGoogle Scholar
Zolovs, M., Deksne, G., Daukšte, J., Aizups, J. & Kirjušina, M. (2016) Morphometric analysis of the hard parts of Pseudodactylogyrus anguillae and Pseudodactylogyrus bini (Monogenea: Dactylogyridae) on the gill apparatus of the European eels (Anguilla anguilla) from the freshwaters of Latvia. Journal of Parasitology 102, 388394.CrossRefGoogle Scholar
Zuur, A., Ieno, E.N., Walker, N., Saveliev, A.A. & Smith, G.M. (2009) Mixed effects models and extensions in ecology with R. 574 pp. New York, USA, Springer Science Business Media.CrossRefGoogle Scholar