Skip to main content
SpringerLink
Log in

Resource contributions from dreissenid mussels to the benthic algae Lyngbya wollei (Cyanobacteria) and Cladophora glomerata (Chlorophyta)

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Dreissena spp. (zebra and quagga mussels) are invasive to North America and increase light to the benthos, provide hard structure for algal attachment, and may contribute limiting nutrients to benthic algae, thereby facilitating algal blooms. We conducted experiments to determine how Dreissena affect nutrient stoichiometry and growth of Lyngbya wollei and Cladophora glomerata, two benthic algal species recently increasing in biomass in parts of the Laurentian Great Lakes, combined with a field survey to determine the likelihood of L. wollei co-occurrence with Dreissena. L. wollei had a significantly higher concentration of carbon, nitrogen, phosphorus, potassium, and sulfur when grown with live Dreissena. C. glomerata had greater biomass in tanks with live Dreissena, but did not have significant increases in nutrient concentration like L. wollei did. Neither algal species increased in growth due to the added structure of Dreissena shells. L. wollei biomass was greater in the presence of Dreissena during 1 year (of two) of our field survey. This field survey also showed that L. wollei and Dreissena are likely to co-occur. These results suggest that Dreissena provide several nutrients to benthic algae, and these added resources can promote algal growth and consequently blooms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams, M. S. & W. Stone, 1973. Field studies on photosynthesis of Cladophora glomerata (Chlorophyta) in Green Bay, Lake Michigan. Ecology 54: 853–862.

    Article  Google Scholar 

  • Albert, S., J. M. O’Neil, J. W. Udy, K. S. Ahern, C. M. O’Sullivan & W. C. Dennison, 2005. Blooms of the cyanobacterium Lyngbya majuscula in coastal Queensland, Australia: disparate sites, common factors. Marine Pollution Bulletin 51: 428–437.

    Article  CAS  PubMed  Google Scholar 

  • Arnott, D. L. & M. J. Vanni, 1996. Nitrogen and phosphorus recycling by the zebra mussel (Dreissena polymorpha) in the western basin of Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 53: 646–659.

    Article  Google Scholar 

  • Auer, M. T., L. M. Tomlinson, S. N. Higgins, S. Y. Malkin, E. T. Howell & H. A. Bootsma, 2010. Great Lakes Cladophora in the 21st century: same algae-different ecosystem. Journal of Great Lakes Research 36: 248–255.

    Article  Google Scholar 

  • Baldwin, B. S., M. S. Mayer, J. Dayton, N. Pau, J. Mendilla, M. Sullivan, A. Moore, A. Ma & E. L. Mills, 2002. Comparative growth and feeding in zebra and quagga mussels (Dreissena polymorpha and Dreissena bugensis): implications for North American Lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 680–694.

    Article  Google Scholar 

  • Barbiero, R. P. & M. L. Tuchman, 2004. Long-term dreissenid impacts on water clarity in Lake Erie. Journal of Great Lakes Research 30: 557–565.

    Article  Google Scholar 

  • Barnes, J. D., L. Balaguer, E. Manrique, S. Elvira & A. W. Davison, 1992. A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany 32: 85–100.

    Article  CAS  Google Scholar 

  • Bootsma, H. A., E. T. Jensen, E. B. Young & J. A. Berges, 2005. Cladophora research and management in the Great Lakes, Proceedings of a Workshop held at the Great Lakes WATER Institute, University of Wisconsin-Milwaukee, 8 December 2004. Great Lakes WATER Institute (GLWI) Special Report No. 2005-01.

  • Botts, P. S., B. A. Patterson & D. W. Schloesser, 1996. Zebra mussel effects on benthic invertebrates: physical or biotic? Journal of the North American Benthological Society 15: 179–184.

    Article  Google Scholar 

  • Bridgeman, T. B. & W. A. Penamon, 2010. Lyngbya wollei in western Lake Erie. Journal of Great Lakes Research 36: 167–171.

    Article  Google Scholar 

  • Bridgeman, T. B., J. D. Chaffin, D. D. Kane, J. D. Conroy, S. E. Panek & P. M. Armenio, 2012. From river to lake: phosphorus partitioning and algal community compositional changes in Western Lake Erie. Journal of Great Lakes Research 38: 90–97.

    Article  CAS  Google Scholar 

  • Camacho, F. A. & R. W. Thacker, 2006. Amphipod herbivory on the freshwater cyanobacterium Lyngbya wollei: chemical stimulants and morphological defenses. Limnology and Oceanography 51: 1870–1875.

    Article  CAS  Google Scholar 

  • Campbell, D., V. Hurry, A. K. Clarke, P. Gustafsson & G. Oquist, 1998. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiology and Molecular Biology Reviews 62: 667–683.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Carmichael, W. W., W. R. Evans, Q. Q. Yin, P. Bell & E. Moczydlowski, 1997. Evidence for paralytic shellfish poisons in the freshwater cyanobacterium Lyngbya wollei (Farlow ex Gomont) comb. nov. Applied and Environmental Microbiology 63: 3104–3110.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Carrick, H. J. & R. L. Lowe, 2007. Nutrient limitation of benthic algae in Lake Michigan: the role of silica. Journal of Phycology 43: 228–234.

    Article  CAS  Google Scholar 

  • Cecala, R. K., C. M. Mayer, K. L. Schulz & E. L. Mills, 2008. Increased benthic algal primary production in response to the invasive zebra mussel (Dreissena polymorpha) in a productive ecosystem, Oneida Lake, New York. Journal of Integrative Plant Biology 50: 1452–1466.

    Article  PubMed  Google Scholar 

  • Chaffin, J. D., 2009. Physiological ecology of Microcystis blooms in turbid waters of western Lake Erie. M.S. Thesis. University of Toledo, Toledo, OH.

  • Cheney, C. & R. A. Hough, 1983. Factors controlling photosynthetic productivity in a population of Cladophora fracta (Chlorophyta). Ecology 64: 68–77.

    Article  Google Scholar 

  • Coakley, J. P., N. Rasul, S. E. Ioannou & G. R. Brown, 2002. Soft sediment as a constraint on the spread of the zebra mussel in western Lake Erie: processes and impacts. Ecosystem Health and Management 5: 329–343.

    Article  Google Scholar 

  • Conroy, J. D., W. J. Edwards, R. A. Pontius, D. D. Kane, H. Zhang, J. F. Shea, J. N. Richey & D. A. Culver, 2005. Soluble nitrogen and phosphorus excretion of exotic freshwater mussels (Dreissena spp.): potential impacts for nutrient remineralization in western Lake Erie. Freshwater Biology 50: 1146–1162.

    Article  CAS  Google Scholar 

  • Cowell, B. C. & P. S. Botts, 1994. Factors influencing the distribution, abundance and growth of Lyngbya wollei in central Florida. Aquatic Botany 49: 1–17.

    Article  CAS  Google Scholar 

  • Dame, R., N. Dankers, T. Prins, H. Jongsma & A. Smaal, 1991. The influence of mussel beds on nutrients in the western Wadden Sea and Eastern Scheldt estuaries. Coastal and Estuarine Research Federation 14: 130–138.

    CAS  Google Scholar 

  • Depew, D. C., A. J. Houben, S. J. Guildford & R. E. Hecky, 2011. Distribution of nuisance Cladophora in the lower Great Lakes: patterns with land use, near shore water quality and dreissenid abundance. Journal of Great Lakes Research 37: 656–671.

    Article  CAS  Google Scholar 

  • Dermott, R. & M. Munawar, 1993. Invasion of Lake Erie offshore sediments by Dreissena, and its ecological implications. Canadian Journal of Fisheries and Aquatic Sciences 50: 2298–2304.

    Article  Google Scholar 

  • Dyck, L. A., 1994. Creation of management strategies that are compatible with the autecology of Lyngbya. Lake and Reservoir Management 9: 71.

    Google Scholar 

  • Fahnenstiel, G. L., T. B. Bridgeman, G. A. Lang, M. J. McCormick & T. F. Nalepa, 1995. Phytoplankton productivity in Saginaw Bay, Lake Huron: effects of zebra mussel (Dreissena polymorpha) colonization. Journal of Great Lakes Research 2: 465–475.

    Google Scholar 

  • Foerster, J. W., 1964. The use of calcium and magnesium hardness ions to stimulate sheath formation in Oscillatoria limosa (Roth) C. A. Agardh. Transactions of the American Microscopical Society 83: 420–427.

    Article  Google Scholar 

  • Furuki, T., S. Maeda, S. Imajo, T. Hiroi, T. Amaya, T. Hirokawa, K. Ito & H. Nozawa, 2003. Rapid and selective extraction of phycocyanin from Spirulina platensis with ultrasonic cell disruption. Journal of Applied Phycology 15: 319–324.

    Article  CAS  Google Scholar 

  • Gerloff, G. C. & G. P. Fitzgerald, 1976. The nutrition of Great Lakes Cladophora. Ecological Research Series EPA-600/3-76-044. U.S. Environmental Protection Agency, Office of Research and Development, Duluth, MN: 111 pp.

  • Government of Canada & United States Environmental Protection Agency, 1995. The Great Lakes: An Environmental Atlas and Resource Book, 3rd ed. Great Lakes National Program Office, Chicago, IL.

    Google Scholar 

  • Guillard, R. R. L. & C. J. Lorenzen, 1972. Yellow-green algae with chlorophyllide c. Journal of Phycology 8: 10–14.

    CAS  Google Scholar 

  • Hebert, R. D. N., B. W. Muncaster & G. L. Mackie, 1989. Ecological and genetic studies on Dreissena polymorpha (Pallas): a new mollusk in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 46: 1587–1591.

    Article  Google Scholar 

  • Hecky, R. E., R. E. H. Smith, D. R. Barton, S. J. Guildford, W. D. Taylor, M. N. Charlton & T. Howell, 2004. The nearshore phosphorus shunt: a consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 61: 1285–1293.

    Article  CAS  Google Scholar 

  • Higgins, S. N., R. E. Hecky & S. J. Guildford, 2005a. Modeling the growth, biomass, and tissue phosphorus concentration of Cladophora glomerata in eastern Lake Erie: model description and field testing. Journal of Great Lakes Research 31: 439–455.

    Article  CAS  Google Scholar 

  • Higgins, S. N., E. T. Howell, R. E. Hecky, S. J. Guildford & R. E. Smith, 2005b. The wall of green: the status of Cladophora glomerata on the northern shores of Lake Erie’s eastern basin, 1995-2002. Journal of Great Lakes Research 31: 547–563.

    Article  Google Scholar 

  • Higgins, S. N., S. Y. Malkin, E. T. Howell, S. J. Guildford, L. Campbell, V. Hiriart-Baer & R. E. Hecky, 2008. An ecological review of Cladophora glomerata (Chlorophyta) in the Laurentian Great Lakes. Journal of Phycology 44: 839–854.

    Article  Google Scholar 

  • Holland, R. E., 1993. Changes in planktonic diatoms and water transparency in Hatchery Bay, Bass Island Area, Western Lake Erie since the establishment of the zebra mussel. Journal of Great Lakes Research 19: 617–624.

    Article  Google Scholar 

  • Kahlert, M., 1998. C:N: P ratios of freshwater benthic algae. Archiv für Hydrobiologie, Special Issues: Ergebnisse der Limnologie, Advances in Limnology 51: 105–114.

    CAS  Google Scholar 

  • Karatayev, A. Y., L. E. Burlakova, C. Pennuto, J. Ciborowski, V. A. Karatayev, P. Juette & M. Clapsadl, 2014. Twenty five years of changes in Dreissena spp. populations in Lake Erie. Journal of Great Lakes Research 40: 550–559.

    Article  Google Scholar 

  • Krug, B. A., B. E. Whipker, J. Frantz & I. McCall, 2009. Characterization of Calcium and Boron deficiency and the effects of temporal disruption of Calcium and Boron supply on Pansy, Petunia, and Gerbera plugs. HortScience 44: 1566–1572.

    Google Scholar 

  • Lowe, R. L. & R. W. Pillsbury, 1995. Shifts in benthic algal community structure and function following the appearance of zebra mussels (Dreissena polymorpha) in Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21: 558–566.

    Article  Google Scholar 

  • Mayer, C. M., R. A. Keats, L. G. Rudstam & E. L. Mills, 2002. Scale-dependent effects of zebra mussels in a large eutrophic lake. Journal of the North American Benthological Society 21: 616–633.

    Article  Google Scholar 

  • Mills, E. L., R. M. Dermott, E. F. Roseman, D. Dustin, E. Mellina, D. B. Conn & A. P. Spidle, 1993. Colonization, ecology, and population structure of the “quagga” mussel (Bivalvia: Dreissenidae) in the lower Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 50: 2305–2314.

    Article  Google Scholar 

  • Nichols, S. J., 1993. Maintenance of the zebra mussel (Dreissena polymorpha) under laboratory conditions. In Nalepa, T. F. & D. W. Schloesser (eds), Zebra Mussels: Biology, Impact, and Control. Lewis Publishers/CRC Press, Boca Raton, FL: 733–747.

    Google Scholar 

  • Ozersky, T., S. Y. Malkin, D. R. Barton & R. E. Hecky, 2009. Dreissenid phosphorus excretion can sustain C. glomerata growth along a portion of Lake Ontario shoreline. Journal of Great Lakes Research 35: 321–328.

    Article  CAS  Google Scholar 

  • Panek, S. E., 2012. The ecology of the nuisance cyanobacterium, Lyngbya wollei, in the western basin of Lake Erie. M.S. Thesis. University of Toledo, Toledo, OH.

  • Peterson, B. J. & K. L. Heck Jr, 1999. The potential for suspension feeding bivalves to increase seagrass productivity. Journal of Experimental Marine Biology and Ecology 240: 37–52.

    Article  Google Scholar 

  • Phlips, E. J., J. Ihnat & M. Conroy, 1992. Nitrogen fixation by the benthic cyanobacterium Lyngbya wollei. Hydrobiologia 234: 59–64.

    Article  Google Scholar 

  • Qin, P., C. M. Mayer, K. L. Schultz & M. E. Ritchie, 2007. Ecological stoichiometry in benthic food webs: effects of light and nutrients on periphyton food quantity and quality in lakes. Limnology and Oceanography 52: 1728–1734.

    Article  CAS  Google Scholar 

  • Reusch, T. B. H., A. R. O. Chapman & J. P. Gröger, 1994. Blue mussels Mytilus edulis do not interfere with eelgrass Zostera marina but fertilize shoot growth through biodeposition. Marine Ecology Progress Series 108: 265–280.

    Article  Google Scholar 

  • Sampath-Wiley, P. & C. D. Neefus, 2007. An improved method for estimating R-phycoerythrin and R-phycocyanin contents from crude aqueous extracts of Porphyra (Bangiales, Rhodophyta). Journal of Applied Phycology 19: 123–129.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sikes, C. S., 1977. Calcium and cation sorption by Cladophora from the Great Lakes. Journal of Great Lakes Research 3: 100–105.

    Article  CAS  Google Scholar 

  • Skubinna, J. P., T. G. Coon & T. R. Batterson, 1995. Increased abundance and depth of submersed macrophytes in response to decreased turbidity in Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21: 476–488.

    Article  Google Scholar 

  • Spivak, A. S., M. J. Vanni & E. M. Mette, 2011. Moving on up: can results from simple aquatic mesocosm experiments be applied across broad spatial scales? Freshwater Biology 56: 279–291.

    Article  Google Scholar 

  • Stevenson, J. C., 1988. Comparative ecology of submersed grass beds in freshwater, estuarine, and marine environments. Limnology and Oceanography 33: 867–893.

    Article  CAS  Google Scholar 

  • Stevenson, R. J., A. Pinowska & Y. Wang, 2004. Ecological condition of algae and nutrients in Florida springs. DEP Contract Number WM858. Final Report. Tallahassee, FL.

  • Thacker, R. W. & V. J. Paul, 2001. Are benthic cyanobacteria indicators of nutrient enrichment? Relationships between cyanobacterial abundance and environmental factors on the reef flats of Guam. Bulletin of Marine Science 69: 497–508.

    Google Scholar 

  • Trick, C. G., S. W. Wilhelm & C. M. Brown, 1995. Alterations in cell pigmentation, protein expression, and photosynthetic capacity of the cyanobacterium Oscillatoria tenuis grown under low iron conditions. Canadian Journal of Microbiology 41: 1117–1123.

    Article  CAS  PubMed  Google Scholar 

  • Vanderploeg, H. A., T. F. Nalepa, D. J. Jude, E. L. Mills, K. T. Holeck, J. R. Liebig, I. A. Grigorovich & H. Ojaveer, 2002. Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1209–1228.

    Article  Google Scholar 

  • Zar, J. H., 1999. Biostatistical Analysis, 4th ed. Prentice Hall, New Jersey.

    Google Scholar 

  • Zhu, B., D. G. Fitzgerald, C. M. Mayer, L. G. Rudstam & E. L. Mills, 2006. Alteration of ecosystem function by zebra mussels in Oneida Lake: impacts on submerged macrophytes. Ecosystems 9: 1017–1028.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Rex Lowe for suggestions during this project, Dr. Jonathan Frantz and the USDA-ARS team at UT for analyzing samples for nutrient content, and Mike Bur and Patrick Kocovsky from USGS for the collection of zebra and quagga mussels. We also wish to thank the Mayer, Bridgeman, and Bossenbroek labs at the University of Toledo for providing lab and field assistance as well as providing constructive comments. Anonymous reviewers were also helpful in the improvement of this manuscript. This research was supported in part by an Ohio Lake Erie Commission Lake Erie Protection Fund Grant to C. Mayer and P. Armenio. This is Contribution Number 2015-04 of the University of Toledo, Lake Erie Center.

Author information

Author notes

  1. Patricia M. Armenio

    Present address: USGS Great Lakes Science Center, 1451 Green Road, Ann Arbor, MI, 48105, USA

Authors and Affiliations

  1. Department of Environmental Sciences and the Lake Erie Center, University of Toledo, 6200 Bayshore Rd., Oregon, OH, 43616, USA

    Patricia M. Armenio, Christine M. Mayer, Thomas B. Bridgeman & Sarah E. Panek

  2. Department of Environmental Sciences, University of Toledo, 2801 W. Bancroft St., Toledo, OH, 43606, USA

    Scott A. Heckathorn

Authors
  1. Patricia M. Armenio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christine M. Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Scott A. Heckathorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas B. Bridgeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sarah E. Panek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patricia M. Armenio.

Additional information

Handling editor: Katya Kovalenko

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 20 kb)

Supplementary material 2 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Armenio, P.M., Mayer, C.M., Heckathorn, S.A. et al. Resource contributions from dreissenid mussels to the benthic algae Lyngbya wollei (Cyanobacteria) and Cladophora glomerata (Chlorophyta). Hydrobiologia 763, 35–51 (2016). https://doi.org/10.1007/s10750-015-2357-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2357-3

Keywords

Search

Navigation