Size-structured vulnerability of the colonial cyanobacterium, Microcystis aeruginosa, to grazing by zebra mussels (Dreissena polymorpha)

Freshwater Biology

Volumn 59, Issue 3, 2014, Pages 514-525

  White, Jeffrey D ^a   Sarnelle, Orlando ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Body size; Colony size; Dreissena polymorpha; Grazing; Microcystis aeruginosa

Indexed keywords

ALGAE; ANKISTRODESMUS; DREISSENA POLYMORPHA; MICROCYSTIS AERUGINOSA;

EID: 84892438220     PISSN: 00465070     EISSN: 13652427     Source Type: Journal    
DOI: 10.1111/fwb.12282     Document Type: Article

References (67)

1. Agrawal A.A. (1998) Algal defense, grazers, and their interactions in aquatic trophic cascades. Acta Oecologica, 19, 331-337.
2. Baker S.M., Levinton J.S., Kurdziel J.P. & Shumway S.E. (1998) Selective feeding and biodeposition by zebra mussels and their relation to changes in phytoplankton composition and seston load. Journal of Shellfish Research, 17, 1207-1213.
3. Bastviken D.T.E., Caraco N.F. & Cole J.J. (1998) Experimental measurements of zebra mussel (Dreissena polymorpha) impacts on phytoplankton community composition. Freshwater Biology, 39, 375-386.
4. Bern L. (1994) Particle selection over a broad size range by crustacean zooplankton. Freshwater Biology, 32, 105-112.
5. Bogdan K.G. & Gilbert J.J. (1984) Body size and food size in freshwater zooplankton. Proceedings of the National Academy of Sciences, 81, 6427-6431.
6. Bozarth C.S., Schwartz A.D., Shepardson J.W., Colwell F.S. & Dreher T.W. (2010) Population turnover in a Microcystis bloom results in predominantly nontoxigenic variants late in the season. Applied and Environmental Microbiology, 76, 5207-5213.
7. Bridoux M., Sobiechowska M., Perez-Fuentetaja A. & Alben K.T. (2010) Algal pigments in Lake Erie dreissenids, pseudofeces and sediments, as tracers of diet, selective feeding and bioaccumulation. Journal of Great Lakes Research, 36, 437-447.
8. Burkholder J.M. & Glibert P.M. (2009) The importance of intraspecific variability in harmful algae- preface to a collection of topical papers. Harmful Algae, 8, 744-745.
9. Burns C.W. (1968) The relationship between body size of filter-feeding Cladocera and the maximum size of particle ingested. Limnology & Oceanography, 13, 675-678.
10. Chislock M.F., Sarnelle O., Jernigan L.M. & Wilson A.E. (2013) Do high concentrations of microcystin prevent Daphnia control of phytoplankton? Water Research, 47, 1961-1970.
11. Cotner J.B., Gardner W.S., Johnson J.R., Sada R.H., Cavaletto J.F. & Heath R.T. (1995) Effects of zebra mussels (Dreissena polymorpha) on bacterioplankton: evidence for both size-selective consumption and growth stimulation. Journal of Great Lakes Research, 21, 517-528.
12. Cyr H. & Pace M.L. (1992) Grazing by zooplankton and its relationship to community structure. Canadian Journal of Fisheries and Aquatic Sciences, 49, 1453-1465.
13. Dionisio Pires L.M., Bontes B.M., Van Donk E. & Ibelings B.W. (2005) Grazing on colonial and filamentous, toxic and non-toxic cyanobacteria by the zebra mussel Dreissena polymorpha. Journal of Plankton Research, 27, 331-339.
14. Dionisio Pires L.M., Jonker R.R., Van Donk E. & Laanbroek H.J. (2004) Selective grazing by adults and larvae of the zebra mussel (Dreissena polymorpha): application of flow cytometry to natural seston. Freshwater Biology, 49, 116-126.
15. Dionisio Pires L.M. & Van Donk E. (2002) Comparing grazing by Dreissena polymorpha on phytoplankton in the presence of toxic and non-toxic cyanobacteria. Freshwater Biology, 47, 1855-1865.
16. Fulton R.S. & Paerl H.W. (1987a) Effects of colonial morphology on zooplankton utilization of algal resourecs during blue-green algal (Microcystis aeruginosa) blooms. Limnology and Oceanography, 32, 634-644.
17. Fulton R.S. & Paerl H.W. (1987b) Toxic and inhibitory effects of the blue-green alga Microcystis aeruginosa on herbivorous zooplankton. Journal of Plankton Research, 9, 837-856.
18. Geller W. & Müller H. (1981) The filtration apparatus of Cladocera: filter mesh-sizes and their implications on food selectivity. Oecologia, 49, 316-321.
19. Hansen B., Bjørnsen P.K. & Hansen P.J. (1994) The size ratio between planktonic predators and their prey. Limnology & Oceanography, 39, 395-403.
20. Higgins S.N. & Vander Zanden M.J. (2010) What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecological Monographs, 91, 179-196.
21. Horgan M.J. & Mills E.L. (1997) Clearance rates and filtering activity of zebra mussel (Dreissena polymorpha): implications for freshwater lakes. Canadian Journal of Fisheries and Aquatic Sciences, 54, 249-255.
22. Idrisi N., Mills E.L., Rudstam L.G. & Stewart D.J. (2001) Impact of zebra mussels (Dreissena polymorpha) on the pelagic lower trophic levels of Oneida Lake, New York. Canadian Journal of Fisheries and Aquatic Sciences, 58, 1430-1441.
23. Jacobs J. (1974) Quantitative measurement of food selection: a modification of the forage ratio and Ivlev's electivity index. Oecologia, 14, 413-417.
24. Jarvis A.C., Hart R.C. & Combrink S. (1987) Zooplankton feeding on size fractionated Microcystis colonies and Chlorella in a hypereutrophic lake (Hartbeesport Dam, South Africa): implications to resource utilization and zooplankton succession. Journal of Plankton Research, 9, 1231-1249.
25. Jarvis A.C., Hart R.C. & Combrink S. (1988) Cladoceran filtration rate-body length relations: model improvements developed for a Microcystis-dominated hypertrophic reservoir. Journal of Plankton Research, 10, 115-131.
26. Jungmann D. & Benndorf J. (1994) Toxicity to Daphnia of a compound extracted from laboratory and natural Microcystis spp., and the role of microcystins. Freshwater Biology, 32, 13-20.
27. Kardinaal W.E.A., Janse I., Kamst-van Agterveld M., Meima M., Snoek J., Mur L.R. et al. (2007) Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquatic Microbial Ecology, 48, 1-12.
28. Knoll L.B., Sarnelle O., Hamilton S.K., Scheele C.E.H., Wilson A.E., Rose J.B. et al. (2008) Invasive zebra mussels (Dreissena polymorpha) increase cyanobacterial toxin concentrations in low-nutrient lakes. Canadian Journal of Fisheries and Aquatic Sciences, 65, 448-455.
29. Kruk C., Huszar V.L.M., Peeters E.T.H.M., Bonilla S., Costa L., Lürling M. et al. (2010) A morphological classification capturing functional variation in phytoplankton. Freshwater Biology, 55, 614-627.
30. Kryger J. & Riisgård H.U. (1988) Filtration rate capacities in 6 species of European freshwater bivalves. Oecologia, 77, 34-38.
31. Lei J., Payne B.S. & Wang S.Y. (1996) Filtration dynamics of the zebra mussel, Dreissena polymorpha. Canadian Journal of Fisheries and Aquatic Sciences, 1995, 29-37.
32. Litchman E. & Klausmeier C.A. (2008) Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution, and Systematics, 39, 615-639.
33. Lund J.W.G., Kipling C. & Cren E.D. (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia, 11, 143-170.
34. MacIsaac H.J., Lonnee C.J. & Leach J.H. (1995) Suppression of microzooplankton by zebra mussels: importance of mussel size. Freshwater Biology, 34, 379-387.
35. MacIsaac H.J., Sprules W.G. & Leach J.H. (1991) Ingestion of small-bodied zooplankton by zebra mussels (Dreissena polymorpha): can cannibalism on larvae influence population dynamics? Canadian Journal of Fisheries and Aquatic Sciences, 48, 2051-2060.
36. McCauley E. & Briand F. (1979) Zooplankton grazing and phytoplankton species richness: field tests of the predation hypothesis. Limnology and Oceanography, 24, 243-252.
37. Naddafi R., Pettersson K. & Eklöv P. (2007) The effect of seasonal variation in selective feeding by zebra mussels (Dreissena polymorpha) on phytoplankton community composition. Freshwater Biology, 52, 823-842.
38. O'Brien K.R., Meyer D.L., Waite A.M., Ivey G.N. & Hamilton D.P. (2004) Disaggregation of Microcystis aeruginosa colonies under turbulent mixing: laboratory experiments in a grid-stirred tank. Hydrobiologia, 519, 143-152.
39. Omori M. & Ikeda T. (1984) Methods in Marine Zooplankton Ecology. John Wiley & Sons, New York, NY.
40. Pitcher G.C. (2012) Harmful algae-The requirement for species-specific information. Harmful Algae, 14, 1-4.
41. R Core Team. (2013) R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria.
42. Raikow D.E., Sarnelle O., Wilson A.E. & Hamilton S.K. (2004) Dominance of the noxious cyanobacterium Microcystis aeruginosa in low nutrient lakes is associated with exotic zebra mussels. Limnology and Oceanography, 49, 482-487.
43. Reynolds C. (2006) Ecology of Phytoplankton. Cambridge University Press, Cambridge.
44. Reynolds C.S., Jaworski G.H.M., Cmiech A. & Leedale G.F. (1981) On the annual cycle of the blue-green alga Microcystis aeruginosa Kütz. Emend. Elenkin. Philosophical Transactions of the Royal Society of London Series B, 293, 419-477.
45. Reynolds C.S. & Rogers D.A. (1976) Seasonal variations in the vertical distribution and buoyancy of Microcystis aeruginosa Kütz. Emend. Elenken in Rostherne Mere, England. Hydrobiologia, 48, 17-23.
46. Rico M., Altamirano M., López-Rodas V. & Costas E. (2006) Analysis of polygenic traits of Microcystis aeruginosa (Cyanobacteria) strains by restricted maximum likelihood (REML) procedures: 1. Size and shape of colonies and cells. Phycologia, 45, 237-242.
47. Rinta-Kanto J.M., Konopko E.A., DeBruyn J.M., Bourbonniere R.A., Boyer G.L. & Wilhelm S.W. (2009) Lake Erie Microcystis: relationships between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae, 8, 665-673.
48. Roditi H.A., Caraco N.F., Cole J.J. & Strayer D.L. (1996) Filtration of Hudson River water by the zebra mussel (Dreissena polymorpha). Estuaries, 19, 824-832.
49. Saker M.L., Fastner J., Dittmann E., Christiansen G. & Vasconcelos V.M. (2005) Variation between strains of the cyanobacterium Microcystis aeruginosa isolated from a Portuguese river. Journal of Applied Microbiology, 99, 749-757.
50. Sandgren C.D. & Robinson J.V. (1984) A stratified sampling approach to compensating for non-random sedimentation of phytoplankton cells in inverted microscope settling chambers. British Phycological Journal, 19, 67-72.
51. Sarnelle O., Morrison J., Kaul R., Horst G., Wandell H. & Bednarz R. (2010) Citizen monitoring: testing hypotheses about the interactive influences of eutrophication and mussel invasion on a cyanobacterial toxin in lakes. Water Research, 44, 141-150.
52. Sarnelle O., White J.D., Horst G.P. & Hamilton S.K. (2012) Phosphorus addition reverses the positive effect of zebra mussels (Dreissena polymorpha) on the toxic cyanobacterium, Microcystis aeruginosa. Water Research, 46, 3471-3478.
53. Sarnelle O., Wilson A.E., Hamilton S.K., Knoll L.B. & Raikow D.E. (2005) Complex interactions between the zebra mussel, Dreissena polymorpha, and the harmful phytoplankter, Microcystis aeruginosa. Limnology and Oceanography, 50, 896-904.
54. Smith T.E., Stevenson R.J., Caraco N.F. & Cole J.J. (1998) Changes in phytoplankton community structure during the zebra mussel (Dreissena polymorpha) invasion of the Hudson River (New York). Journal of Plankton Research, 20, 1567-1579.
55. Sprules W.G., Casselman J.M. & Shuter B.J. (1983) Size distribution of pelagic particles in lakes. Canadian Journal of Fisheries and Aquatic Sciences, 40, 1761-1769.
56. Sprung M. & Rose U. (1988) Influence of food size and food quantity on the feeding of the mussel Dreissena polymorpha. Oecologia, 77, 526-532.
57. Sterner R.W. (1989) The role of grazers in phytoplankton succession. In: Plankton Ecology: Succession in Plankton Communities. (Ed. U. Sommer ), pp. 107-170. Springer-Verlag, Berlin, Germany.
58. Strayer D.L. (2008) Twenty years of zebra mussels: lessons from the mollusk that made headlines. Frontiers in Ecology and the Environment, 7, 135-141.
59. Ten Winkel E.H. & Davids C. (1982) Food selection by Dreissena polymorpha Pallas (Mollusca: Bivalvia). Freshwater Biology, 12, 553-558.
60. Vanderploeg H.A., Liebig J.R., Carmichael W.W., Agy M.A., Johengen T.H., Fahnenstiel G.L. et al. (2001) Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences, 58, 1208-1221.
61. Visser P.M., Passarge J. & Mur L.R. (1997) Modelling vertical migration of the cyanobacterium Microcystis. Hydrobiologia, 349, 99-109.
62. Welker M., Šejnohová L., Némethová D., von Hans D., Jarkovský J. & Maršálek B. (2007) Seasonal shifts in chemotype composition of Microcystis sp. communities in the pelagial and the sediment of a shallow reservoir. Limnology and Oceanography, 52, 609-619.
63. Welschmeyer N.A. (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and phaeopigments. Limnology and Oceanography, 39, 1985-1992.
64. White J.D., Kaul R.B., Knoll L.B., Wilson A.E. & Sarnelle O. (2011) Large variation in vulnerability to grazing within a population of the colonial phytoplankter, Microcystis aeruginosa. Limnology and Oceanography, 56, 1714-1724.
65. Wilson A.E., Kaul R.B. & Sarnelle O. (2010) Growth rate consequences of coloniality in a harmful phytoplankter. PLoS ONE, 5, e8679.
66. Wilson A.E. & Sarnelle O. (2002) Relationship between zebra mussel biomass and total phosphorus in European and North American lakes. Archiv fur Hydrobiologie, 153, 339-351.
67. Wilson A.E., Wilson W.A. & Hay M.E. (2006) Intraspecific variation in growth and morphology of the bloom-forming cyanobacterium Microcystis aeruginosa. Applied and Environmental Microbiology, 72, 7386-7389.