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Freshwater mussels (Anodonta anatina) reduce transmission of a common fish trematode (eye fluke, Diplostomum pseudospathaceum)

Published online by Cambridge University Press:  02 August 2017

M. GOPKO
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninskij prosp., 33, 119071 Moscow, Russia
E. MIRONOVA*
Affiliation:
Institute of Cytology of the Russian Academy of Sciences, Tikhoretsky Ave., 4, 194064 Saint Petersburg, Russia
A. PASTERNAK
Affiliation:
P. P. Shirshov Institute of Oceanology of the Russian Academy of Sciences, Nakhimovskii prosp., 36, 117997 Moscow, Russia
V. MIKHEEV
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninskij prosp., 33, 119071 Moscow, Russia
J. TASKINEN
Affiliation:
Department of Biological and Environmental Science P.O. Box 35, University of Jyväskylä, FIN-40014, Finland
*
*Corresponding author: Institute of Cytology of the Russian Academy of Sciences, Tikhoretsky Ave., 4, 194064 Saint Petersburg, Russia. E-mail: katya_mironova@mail.ru

Summary

Recent results suggest that bivalves can play an important role in restraining the spread of various aquatic infections. However, the ability of mussels to remove free-living stages of macroparasites and reduce their transmission is still understudied, especially for freshwater ecosystems. We investigated the influence of the common freshwater mussel (Anodonta anatina) on the transmission of a trematode (eye fluke, Diplostomum pseudospathaceum), which frequently infects fish in farms and natural habitats. In our experiments, mussels caused a significant decrease (P < 0·001) in the abundance of trematode free-living stages, from 6520 to 1770 cercariae L−1 on average (about 4-fold in 2 h). Individual clearance rates of mussels were 0·6‒3·7 L per hour (mean 1·9). These tests were followed by experimental infections of rainbow trout (Oncorhynchus mykiss) with different doses of D. pseudospathaceum cercariae in the presence or absence of mussels. Exposure of fish to cercariae in the presence of mussels significantly (P < 0·05) reduced the infection intensities in fish (by 30–40%) at all exposure doses. Our results indicate that freshwater bivalves can markedly reduce local cercariae densities and could be useful in mitigation of trematodoses harmful to fish farming.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

These authors are joint first authors.

References

REFERENCES

Alexander, N. (2012). Analysis of parasite and other skewed counts. Tropical Medicine and International Health 17, 684693.Google Scholar
Barnhart, M. C. (2006). Buckets of muckets: a compact system for rearing juvenile freshwater mussels. Aquaculture 254, 227233.Google Scholar
Bartsch, A., Robinson, S. M. C., Liutkus, M., Ang, K. P., Webb, J. and Pearce, C. M. (2013). Filtration of sea louse, Lepeophtheirus salmonis, copepodids by the blue mussel, Mytilus edulis, and the Atlantic sea scallop, Placopecten magellanicus, under different flow, light and copepodid-density regimes. Journal of Fish Diseases 36, 361370.Google Scholar
Burge, C. A., Closek, C. J., Friedman, C. S., Groner, M. L., Jenkins, C. M., Shore-Maggio, A. and Welsh, J. E. (2016). The use of filter-feeders to manage disease in a changing world. Integrative and Comparative Biology 56, 573587.Google Scholar
Conn, D. B. and Conn, D. A. (1995). Experimental infection of zebra mussels Dreissena polymorpha (Mollusca: Bivalvia) by metacercariae of Echinoparyphium sp. (Platyhelminthes: Trematoda). The Journal of Parasitology 81, 304305.Google Scholar
Conn, D. B., Lucy, F. E. and Graczyk, T. K. (2013). Dreissenid mussels as sentinel biomonitors for human and zoonotic pathogens. In Quagga and Zebra Mussels: Biology, Impacts, and Control, 2nd Edn. (ed. Nalepa, T. F. and Schloesser, D. W.), pp. 265272. CRC Press, Boca Raton, USA.Google Scholar
Conover, R. J. (1978). Transformation of organic matter. In Marine Ecology, vol. 4, (ed. Kinne, O.), Dynamics, pp. 221499. Wiley, New York, USA.Google Scholar
Crowden, A. E. and Broom, D. M. (1980). Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour 28, 287294.CrossRefGoogle Scholar
Englund, V. P. M. and Heino, M. P. (1996). Valve movement of the freshwater mussel Anodonta anatina: a reciprocal transplant experiment between lake and river. Hydrobiologia 328, 4956.Google Scholar
Eversole, A. G., Stuart, K. R. and Brune, D. E. (2008). Effect of temperature and phytoplankton concentration of partitioned aquaculture system water on freshwater mussel filtration. Aquaculture Research 39, 16911696.Google Scholar
Faust, C., Stallknecht, D., Swayne, D. and Brown, J. (2009). Filter-feeding bivalves can remove avian influenza viruses from water and reduce infectivity. Proceedings of the Royal Society of London B: Biological Sciences 276, 37273735.Google Scholar
Fenwick, A. (2012). The global burden of neglected tropical diseases. Public Health 126, 233236.Google Scholar
Fried, B., Emili, S. and Ettinger, W. S. (1987). Experimental infection of Corbicula fluminea (Bivalvia: Corbiculidae) with Echinostoma revolutum cercariae. Journal of Parasitology 73, 655656.CrossRefGoogle ScholarPubMed
Frost, B. W. (1972). Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus . Limnology Oceanography 17, 805815.Google Scholar
Gibson, D. I., Taskinen, J. and Valtonen, E. T. (1992). Studies on bucephalid digeneans parasitising molluscs and fishes in Finland. II. The description of Rhipidocotyle fennica n. sp. and its discrimination by principal component analysis. Systematic Parasitology 23, 6779.Google Scholar
Goedknegt, M. A., Welsh, J. E., Drent, J. and Thieltges, D. W. (2015). Climate change and parasite transmission: how temperature affects parasite infectivity via predation on infective stages. Ecosphere 6, 19.Google Scholar
Gopko, M., Mikheev, V. N. and Taskinen, J. (2015). Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis. Behavioral Ecology and Sociobiology 69, 17231730.CrossRefGoogle Scholar
Gopko, M., Mikheev, V. N. and Taskinen, J. (2017). Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae. Behavioral Ecology and Sociobiology 71, 68.Google Scholar
Gosling, E. (2003). Bivalve Molluscs: Biology, Ecology and Culture. Blackwell Publishing Ltd, Oxford, USA.Google Scholar
Graczyk, T. K., Conn, D. B., Lucy, F., Minchin, D., Tamang, L., Moura, L. N. S. and DaSilva, A. G. (2004). Human waterborne parasites in zebra mussels (Dreissena polymorpha) from the Shannon River drainage area, Ireland. Parasitology Research 93, 385391.Google Scholar
Hänninen, M. L., Hörman, A., Rimhanen-Finne, R., Vahtera, H., Malmberg, S., Herve, S. and Lahti, K. (2005). Monitoring of Cryptosporidium and Giardia in the Vantaa river basin, southern Finland. International Journal of Hygiene and Environmental Health 208, 163171.Google Scholar
Hanson, J. M., Mackay, W. C. and Prepas, E. E. (1988). Population size, growth, and production of a unionid clam, Anodonta grandis simpsoniana, in a small, deep boreal forest lake in central Alberta. Canadian Journal of Zoology 66, 247253.Google Scholar
Hawkins, L. A., Armstrong, J. D. and Magurran, A. E. (2004). Predator-induced hyperventilation in wild and hatchery Atlantic salmon fry. Journal of Fish Biology 65 (Suppl. A), 88100.Google Scholar
Hawkins, L. A., Magurran, A. E. and Armstrong, J. D. (2007). Innate abilities to distinguish between predator species and cue concentration in Atlantic salmon. Animal Behaviour. 73, 10511057.Google Scholar
Huyvaert, K. P., Carlson, J. S., Bentler, K. T., Cobble, K. R., Nolte, D. L. and Franklin, A. B. (2012). Freshwater clams as bioconcentrators of avian influenza virus in water. Vector Borne Zoonotic Diseases 12, 904906.Google Scholar
Ismail, N. S., Dodd, H., Sassoubre, L. M., Horne, A. J., Boehm, A. B. and Luthy, R. G. (2015). Improvement of urban lake water quality by removal of Escherichia coli through the action of the bivalve Anodonta californiensis . Environmental Science and Technology 49, 16641672.Google Scholar
Johnson, P. T. G., Dobson, A., Lafferty, K. D., Marcogliese, D. G., Memmott, J., Orlofske, S. A., Poulin, R. and Thieltges, D. W. (2010). When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology and Evolution 25, 362371.Google Scholar
Jokela, J. and Palokangas, P. (1993). Reproductive tactics in Anodonta clams: parental host recognition. Animal Behaviour 46, 618620.Google Scholar
Karvonen, A., Seppälä, O. and Valtonen, E. T. (2004 a). Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129, 473478.Google Scholar
Karvonen, A., Kirsi, S., Hudson, P. and Valtonen, E. (2004 b). Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology 129, 8792.CrossRefGoogle ScholarPubMed
Karvonen, A., Savolainen, M., Seppälä, O. and Valtonen, E. T. (2006). Dynamics of Diplostomum spathaceum infection in snail hosts at a fish farm. Parasitology Research 99, 341345.Google Scholar
Karvonen, A., Aalto-Araneda, M., Virtala, A.-M., Kortet, R., Koski, P. and Hyvärinen, P. (2016). Enriched rearing environment and wild genetic background can enhance survival and disease resistance of salmonid fishes during parasite epidemics. Journal of Applied Ecology 53, 213221.Google Scholar
Kim, B.-H., Lee, U.-H. and Hwang, S.-G. (2011). Inter- and intra-specific differences in filtering activities between two unionids, Anodonta woodiana and Unio douglasiae, in ambient eutrophic lake waters. Ecological Engineering 37, 19571967.Google Scholar
King, S. and Scholz, T. Š. (2001). Trematodes of the family Opisthorchiidae: a minireview. Korean Journal of Parasitology 39, 209221.Google Scholar
Kryger, J. and Riisgård, H. U. (1988). Filtration rate capacities in 6 species of European freshwater bivalves. Oecologia 77, 3438.Google Scholar
Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K., Aguirre-Macedo, L., Boch, C., Dobson, A., Dunham, E. J., Fredensborg, B. L., Huspeni, T. C., Lorda, J., Mababa, L., Mancini, F., Mora, A., Pickering, M., Talhouk, N., Torchin, M. E. and Lafferty, K. D. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515518.Google Scholar
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T. J., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R. and Thieltges, D. W. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533546.Google Scholar
Lopes-Lima, M., Sousa, R., Geist, J., Aldridge, D. C., Araujo, R., Bergengren, J., Bespalaya, Y., Bódis, E., Burlakova, L., Van Damme, D., Douda, K., Froufe, E., Georgiev, D., Gumpinger, C., Karatayev, A., Kebapçi, Ü., Killeen, I., Lajtner, J., Larsen, B. M., Lauceri, R., Legakis, A., Lois, S., Lundberg, S., Moorkens, E., Motte, G., Nagel, K.-O., Ondina, P., Outeiro, A., Paunovic, M., Prié, V. et al. (2016). Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biological Reviews 92, 572607.Google Scholar
Lucy, F. E., Graczyk, T. K., Tamang, L., Miraflor, A. and Minchin, D. (2008). Biomonitoring of surface and coastal water for Cryptosporidium, Giardia, and human-virulent microsporidia using molluscan shellfish. Parasitology Research 103, 13691375.Google Scholar
Lyholt, H. C. K. and Buchmann, K. (1996). Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms 25, 169173.Google Scholar
McIvor, A. L. (2004). Freshwater mussels as biofilters. PhD thesis. Department of Zoology, University of Cambridge.Google Scholar
McLaughlan, C. and Aldridge, D. C. (2013). Cultivation of zebra mussels (Dreissena polymorpha) within their invaded range to improve water quality in reservoirs. Water Research 47, 43574369.Google Scholar
McMahon, R. F. (1991). Mollusca: bivalvia. In Ecology and Classification of North American Freshwater Invertebrates (ed. Thorp, J. H. and Covich, A. P.), pp. 331429. Academic Press, San Diego, USA.Google Scholar
Mezzanotte, V., Marazzi, F., Bissa, M., Pacchioni, S., Binelli, A., Parolini, M., Magni, S., Ruggeri, F. M., Morghen, C. G., Zanotto, C. and Radaelli, A. (2016). Removal of enteric viruses and Escherichia coli from municipal treated effluent by zebra mussels. Science of the Total Environment 539, 395400.Google Scholar
Mikheev, V. N., Afonina, M. O. and Pavlov, D. S. (2010 a). Habitat heterogeneity and fish behaviour: units of heterogeneity as a resource and as a source of information. Journal of Ichthyology 50, 386395.Google Scholar
Mikheev, V. N., Pasternak, A. F., Taskinen, J. and Valtonen, E. T. (2010 b). Parasite-induced aggression and impaired contest ability in a fish host. Parasites and Vectors 3, 17.Google Scholar
Mikheev, V. N., Pasternak, A. F. and Valtonen, E. T. (2014). Increased ventilation by fish leads to a higher risk of parasitism. Parasites and Vectors 7, 281.Google Scholar
Miller, W. A., Miller, M. A., Gardner, I. A., Atwill, E. R., Byrne, B. A., Jang, S., Harris, M., Ames, J., Jessup, D., Paradies, D., Worcester, K., Melli, A. and Conrad, P. A. (2006). Salmonella spp., Vibrio spp., Clostridium perfringens, and Plesiomonas shigelloides in marine and freshwater invertebrates from coastal California ecosystems. Microbial Ecology 52, 198206.Google Scholar
Molloy, S. D., Pietrak, M. R., Bouchard, D. A. and Bricknell, I. (2011). Ingestion of Lepeophtheirus salmonis by the blue mussel Mytilus edulis . Aquaculture 311, 6164.Google Scholar
Morley, N. (2012). Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 719.Google Scholar
Orlofske, S. A., Jadin, R. C., Preston, D. L. and Johnson, P. T. G. (2012). Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93, 12471253.Google Scholar
Orlofske, S. A., Jadin, R. C. and Johnson, P. T. J. (2015). It's a predator-eat-parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178, 537547.Google Scholar
Oulasvirta, P. (2011). Distribution and status of the freshwater pearl mussel Margaritifera margaritifera in northern Fennoscandia. Toxicological and Environmental Chemistry 93, 17131730.Google Scholar
Owen, S. F., Barber, I. and Hart, P. J. B. (1993). Low level infection by eye fluke, diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus . Journal of Fish Biology 42, 803806.Google Scholar
Pusch, M., Siefert, J. and Walz, N. (2001). Filtration and respiration rates of two unionid species and their impact on the water quality of a lowland river. In Ecology and Evolution of the Freshwater Mussels Unionoida (ed. Bauer, G. and Wachtler, K.), Ecological Studies Series, vol. 145, pp. 317326. Springer-Verlag, Berlin Heidelberg, DE.Google Scholar
R Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ Google Scholar
Robertson, L. J. (2007). The potential for marine bivalve shellfish to act as transmission vehicles for outbreaks of protozoan infections in humans: a review. International Journal of Food Microbiology 120, 201216.Google Scholar
Ross, A. G., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y., Williams, G. M. and McManus, D. P. (2002). Schistosomiasis. New England Journal of Medicine 346, 12121220.Google Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2004). Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Animal Behavior 68, 257263.Google Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2005). Impaired crypsis of fish infected with a trophically transmitted parasite. Animal Behavior 70, 895900.Google Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2008). Shoaling behavior of fish under parasitism and predation risk. Animal Behavior 75, 145150.Google Scholar
Schotthoefer, A. M., Labak, K. M. and Beasley, V. R. (2007). Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators. Journal of Parasitology 93, 12401243.Google Scholar
Scriven, K., Jones, H., Taylor, J., Aldridge, D. C. and McIvor, A. (2011). A novel system for rearing freshwater pearl mussels, margaritifera margaritifera (bivalvia, margaritiferidae), at mawddach fish hatchery in wales, UK. In Rearing of Unionoid Mussels (with Special Emphasis on the Freshwater Pearl Mussel Margaritifera Margaritifera) (ed. Frank, T.), Ferrantia 64, pp. 2329. Musée national d'histoire naturelle, Luxembourg, LU.Google Scholar
Shinn, A. P., Pratoomyot, J., Bron, J. E., Paladini, G., Brooker, E. E. and Brooker, A. J. (2015). Economic costs of protistan and metazoan parasites to global mariculture. Parasitology 142, 196270.CrossRefGoogle ScholarPubMed
Słodkowicz-Kowalska, A., Majewska, A. C., Rzymski, P., Skrzypczak, L. and Werner, A. (2015). Human waterborne protozoan parasites in freshwater bivalves (Anodonta anatina and Unio tumidus) as potential indicators of fecal pollution in urban reservoir. Limnologica 51, 3236.Google Scholar
Sokolov, S. G. (2010). Parasites of underyearling kamchatka mykiss Parasalmo mykiss mykiss (Osteichithyes: Salmonidae) in the Utkholok River. North-Western Kamchatka Parazitologiia 44, 336342 (in Russian).Google Scholar
StatSoft, Inc. (2011). STATISTICA (Data Analysis Software System), version 10. Tulsa, OK, USA. http://www.statsoft.com/ Google Scholar
Stumpf, P., Failing, K., Papp, T., Nazir, J., Böhm, R. and Marschang, R. E. (2010). Accumulation of a low pathogenic avian influenza virus in zebra mussels (Dreissena polymorpha). Avian Diseases 54, 11831190.Google Scholar
Stybel, N., Fenske, C. and Schernewski, G. (2009). Mussel cultivation to improve water quality in the Szczecin Lagoon. Journal of Coastal Research 56, 14591463.Google Scholar
Taskinen, J. and Valtonen, E. T. (1995). Age-, size-, and sex-specific infection of Anodonta piscinalis (Bivalvia: Unionidae) with Rhipidocotyle fennica (Digenea: Bucephalidae) and its influence on host reproduction. Canadian Journal of Zoology 73, 887897.Google Scholar
Taskinen, J., Valtonen, E. T. and Gibson, D. I. (1991). Studies on bucephalid digeneans parasitising molluscs and fishes in Finland. I. Ecological data and experimental studies. Systematic Parasitology 19, 8194.Google Scholar
Thieltges, D. W., Jensen, K. T. and Poulin, R. (2008 a). The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407426.Google Scholar
Thieltges, D. W., de Montaudouin, X., Fredensborg, B., Jensen, K. T., Koprivnikar, J. and Poulin, R. (2008 b). Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Marine Ecology Progress Series 372, 147155.Google Scholar
Thieltges, D. W., Reise, K., Prinz, K. and Jensen, K. T. (2009). Invaders interfere with native parasite–host interactions. Biological Invasions 11, 14211429.Google Scholar
Valtonen, E. T. and Gibson, D. I. (1997). Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities of northern Finland. Annales Zoologici Fennici 34, 4759.Google Scholar
Vanderploeg, H. A., Liebig, J. R. and Nalepa, T. F. (1995). From picoplankton to microplankton: temperature-driven filtration by the unionid bivalve Lampsilis radiata siliquoidea in Lake St. Clair. Canadian Journal of Fisheries and Aquatic Sciences 52, 6374.Google Scholar
Voutilainen, A., Saarinen, M., Suonpää, A. and Taskinen, J. (2009). In vitro efficacy of praziquantel against the cercariae of Diplostomum sp., Rhipidocotyle fennica and R. Campanula . Journal of Fish Diseases, 32, 907909.Google Scholar
Welsh, J. E., van der Meer, J., Brussaard, C. P. D. and Thieltges, D. W. (2014). Inventory of organisms interfering with transmission of a marine trematode. Journal of the Marine Biological Association of the United Kingdom 94, 697702.Google Scholar
Wickham, H. (2009). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York, USA.Google Scholar
Willis, J. E., McClure, J. T., McClure, C., Spears, J., Davidson, J. and Greenwood, S. J. (2014). Bioaccumulation and elimination of Cryptosporidium parvum oocysts in experimentally exposed Eastern oysters (Crassostrea virginica) held in static tank aquaria. International Journal of Food Microbiology 173, 7280.Google Scholar
Wilson, K., Bjornstad, O. N., Dobson, A. P., Merler, S., Po-Glayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizolli, A., Grenfell, B. T., Heester-Beek, H. and Dobson, A. P.), pp. 644. Oxford University Press, New York, USA.Google Scholar
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