Mapping the spatial distribution of the biomass and filter-feeding effect of invasive dreissenid mussels on the winter-spring phytoplankton bloom in Lake Michigan

Freshwater Biology

Volumn 60, Issue 11, 2015, Pages 2270-2285

  Rowe, Mark D ^a,b   Obenour, Daniel R ^b,c   Nalepa, Thomas F ^a,b   Vanderploeg, Henry A ^a   Yousef, Foad ^d   Kerfoot, W Charles ^d  

^a NOAA GREAT LAKES ENVIRONMENTAL RESEARCH LABORATORY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c North Carolina State University   (United States)

^d MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

Author keywords

Benthos; GIS; Invasive species; Invertebrates; Lakes; Modelling; Physical environment; Population; Statistics

Indexed keywords

EID: 84943354248     PISSN: 00465070     EISSN: 13652427     Source Type: Journal    
DOI: 10.1111/fwb.12653     Document Type: Article

References (55)

1. Auer M., Tomlinson L., Higgins S., Malkin S., Howell E. & Bootsma H. (2010) Great Lakes Cladophora in the 21st century: same algae-different ecosystem. Journal of Great Lakes Research, 36, 248-255.
2. Auer M.T., Auer N.A., Urban N.R. & Auer T. (2013) Distribution of the amphipod Diporeia in lake superior: the ring of fire. Journal of Great Lakes Research, 39, 33-46.
3. Beletsky D. & Schwab D. (2001) Modeling circulation and thermal structure in Lake Michigan: annual cycle and interannual variability. Journal of Geophysical Research, 106, 19745-19771.
4. Beletsky D., Schwab D. & McCormick M. (2006) Modeling the 1998-2003 summer circulation and thermal structure in Lake Michigan. Journal of Geophysical Research, 111, 1-18.
5. Benson A.J. (2014) Chronological history of zebra and quagga mussels (Dreissenidae) in North America, 1988-2010. In: Quagga and Zebra Mussels: Biology, Impacts, and Control. (Eds T.F. Nalepa & D.W. Schloesser), pp. 9-29. CRC Press, Boca Raton.
6. Box G.E. & Cox D.R. (1964) An analysis of transformations. Journal of the Royal Statistical Society. Series B (Methodological), 26(2), 211-252.
7. Brown J.E. & Stepien C.A. (2010) Population genetic history of the dreissenid mussel invasions: expansion patterns across North America. Biological invasions, 12, 3687-3710.
8. Chiles J.P. & Delfiner P. (2009) Geostatistics: Modeling Spatial Uncertainty. John Wiley & Sons, New York.
9. Connelly N.A., O'Neill C.R. Jr, Knuth B.A. & Brown T.L. (2007) Economic impacts of zebra mussels on drinking water treatment and electric power generation facilities. Environmental Management, 40, 105-112.
10. Coordinating Committee on Great Lakes Basic Hydraulic and Hydrologic Data. (1977) Coordinated Great Lakes Physical Data. Chicago, IL and Cornwall, ON. pp. 9.
11. Diggle P. & Ribeiro P. Jr. (2007) Model-based Geostatistics. Springer, New York.
12. Fahnenstiel G., Nalepa T., Pothoven S., Carrick H. & Scavia D. (2010a) Lake Michigan lower food web: long-term observations and Dreissena impact. Journal of Great Lakes Research, 36, 1-4.
13. Fahnenstiel G.L., Pothoven S., Vanderploeg H., Klarer D., Nalepa T. & Scavia D. (2010b) Recent changes in primary production and phytoplankton in the offshore region of southeastern Lake Michigan. Journal of Great Lakes Research, 36, 20-29.
14. Fahnenstiel G.L. & Scavia D. (1987) Dynamics of Lake Michigan phytoplankton: recent changes in surface and deep communities. Canadian Journal of Fisheries and Aquatic Sciences, 44, 509-514.
15. Fahnenstiel G.L., Stone R.A., McCormick M.J., Schelske C.L. & Lohrenz S.E. (2000) Spring isothermal mixing in the Great Lakes: evidence of nutrient limitation and nutrient-light interactions in a suboptimal light environment. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1901-1910.
16. Hecky R., Smith R.E., Barton D., Guildford S., Taylor W., Charlton M. et al. (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.
17. 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, 80, 179-196.
18. Houghton J.S., Paddock R. & Janssen J. (2014) Invasion of quagga mussels (Dreissena rostriformis bugensis) to the mid-lake reef complex in Lake Michigan: a photographic montage. In: Quagga and Zebra Mussels: Biology, Impacts, and Control. (Eds T.F. Nalepa & D.W. Schloesser), pp. 65-70. CRC Press, Boca Raton.
19. Jardim E. & Ribeiro P.J. Jr. (2007) Geostatistical assessment of sampling designs for Portuguese bottom trawl surveys. Fisheries Research, 85, 239-247.
20. Jardim E. & Ribeiro P.J. Jr. (2008) Geostatistical tools for assessing sampling designs applied to a Portuguese bottom trawl survey field experience. Scientia Marina, 72, 623-630.
21. Karatayev A.Y., Burlakova L.E., Mastitsky S.E., Padilla D.K. & Mills E.L. (2011) Contrasting rates of spread of two congeners, Dreissena polymorpha and Dreissena rostriformis bugensis, at different spatial scales. Journal of Shellfish Research, 30, 923-931.
22. Karatayev A.Y., Burlakova L.E. & Padilla D.K. (2002) Impacts of zebra mussels on aquatic communities and their roles as ecosystem engineers. In: Invasive Aquatic Species of Europe. Distribution, Impacts and Management. (Eds E. Leppa-koski, S. Gollash, and S. Olenin), pp. 433-446. Kluwer Academic Publishers, Dordrecht, The Netherlands.
23. Karatayev A.Y., Burlakova L.E. & Padilla D.K. (2014) Zebra versus quagga mussels: a review of their spread, population dynamics, and ecosystem impacts. Hydrobiologia, 746(1), 1-16.
24. Kerfoot W.C., Budd J.W., Green S.A., Cotner J.B., Biddanda B.A., Schwab D.J. et al. (2008) Doughnut in the desert: late-winter production pulse in southern Lake Michigan. Limnology and Oceanography, 53, 589.
25. Kerfoot W.C., Yousef F., Green S.A., Budd J.W., Schwab D.J. & Vanderploeg H.A. (2010) Approaching storm: disappearing winter bloom in Lake Michigan. Journal of Great Lakes Research, 36, 30-41.
26. Lesht B.M., Barbiero R.P. & Warren G.J. (2013) A band-ratio algorithm for retrieving open-lake chlorophyll values from satellite observations of the Great Lakes. Journal of Great Lakes Research, 39, 138-152.
27. Madenjian C.P., Pothoven S.A., Dettmers J.M. & Holuszko J.D. (2006) Changes in seasonal energy dynamics of alewife (Alosa pseudoharengus) in Lake Michigan after invasion of dreissenid mussels. Canadian Journal of Fisheries and Aquatic Sciences, 63, 891-902.
28. Muggeo V.M.R. (2003) Estimating regression models with unknown break-points. Statistics in medicine, 22, 3055-3071.
29. Muggeo V.M.R. (2008) Segmented: an R package to fit regression models with broken-line relationships. R News, 8, 20-25.
30. Nalepa T.F., Cavaletto J.F., Ford M., Gordon W.M. & Wimmer M. (1993) Seasonal and annual variation in weight and biochemical content of the zebra mussel, Dreissena polymorpha, in Lake St. Clair. Journal of Great Lakes Research, 19, 541-552.
31. Nalepa T.F., Fanslow D.L. & Lang G.A. (2009) Transformation of the offshore benthic community in Lake Michigan: recent shift from the native amphipod Diporeia spp. to the invasive mussel Dreissena rostriformis bugensis. Freshwater Biology, 54, 466-479.
32. Nalepa T.F., Fanslow D.L., Lang G.A., Lamarand D.B., Cummins L.G. & Carter G.S. (2008) Abundances of the amphipod Diporeia spp. and the mussels Dreissena polymorpha and Dreissena rostriformis bugensis in Lake Michigan in 1994-1995, 2000, and 2005. NOAA Technical Memorandum GLERL-144, Ann Arbor, Michigan, USA, p. 25, URL: http://www.glerl.noaa.gov/ftp/publications/tech_reports/glerl-144/tm-144.pdf.
33. Nalepa T.F., Fanslow D.L., Mabrey K., Lang G.A. & Rowe M.D. (2014) Lake-wide benthic surveys in Lake Michigan in 1994-1995, 2005, 2005, and 2010: Abundances of the amphipod Diporeia spp., and abundances and biomass of mussels Dreissena polymorpha and Dreissena rostriformis bugensis. NOAA Technical Memorandum GLERL-164, Ann Arbor, Michigan, USA, p. 25, URL: http://www.glerl.noaa.gov/ftp/publications/tech_reports/glerl-164/tm-164.pdf.
34. Nalepa T.F., Fanslow D.L. & Pothoven S.A. (2010) Recent changes in density, biomass, recruitment, size structure, and nutritional state of Dreissena populations in southern Lake Michigan. Journal of Great Lakes Research, 36, 5-19.
35. Nalepa T.F., Schloesser D.W., Pothoven S.A., Hondorp D.W., Fanslow D.L., Tuchman M.L. et al. (2001) First finding of the amphipod Echinogammarus ischnus and the mussel Dreissena bugensis in Lake Michigan. Journal of Great Lakes Research, 27, 384-391.
36. Obenour D.R., Gronewold A.D., Stow C.A. & Scavia D. (2014) Using a Bayesian hierarchical model to improve Lake Erie cyanobacteria bloom forecasts. Water Resources Research, 50, 7847-7860.
37. Obenour D.R., Scavia D., Rabalais N.N., Turner R.E. & Michalak A.M. (2013) Retrospective analysis of midsummer hypoxic area and volume in the northern Gulf of Mexico, 1985-2011. Environmental Science & Technology, 47, 9808-9815.
38. Pothoven S.A., Fahnenstiel G.L. & Vanderploeg H.A. (2010) Temporal trends in Mysis relicta abundance, production, and life-history characteristics in southeastern Lake Michigan. Journal of Great Lakes Research, 36, 60-64.
39. R Core Team. (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available at: http://www.R-project.org/.
40. Ribeiro P.J. Jr, Christensen O.F. & Diggle P.J. (2003) geoR and geoRglm: software for model-based geostatistics. In: Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003), Vienna, Austria. (Eds. K. Hornik, L. Friedrich & Z. Achim), pp. 1-16. R project, http://www.r-project.org/conferences/DSC-2003/Proceedings/.
41. Ribeiro P.J. Jr. & Diggle P.J. (2001) geoR: a package for geostatistical analysis. R-NEWS, 1, 15-18.
42. Schummer M.L., Petrie S.A. & Bailey R.C. (2008) Dietary overlap of sympatric diving ducks during winter on northeastern Lake Ontario. The Auk, 125, 425-433.
43. Schwarz G. (1978) Estimating the dimension of a model. The Annals of Statistics, 6, 461-464.
44. Shuchman R.A., Leshkevich G., Sayers M.J., Johengen T.H., Brooks C.N. & Pozdnyakov D. (2013) An algorithm to retrieve chlorophyll, dissolved organic carbon, and suspended minerals from Great Lakes satellite data. Journal of Great Lakes Research, 39, 14-33.
45. Sibson R. (1981) A brief description of natural neighbour interpolation. In: Interpreting Multivariate Data. (Ed Barnett V.), pp. 21-36. Wiley, New York.
46. Siegel D., Doney S. & Yoder J. (2002) The North Atlantic spring phytoplankton bloom and Sverdrup's critical depth hypothesis. Science, 296, 730-733.
47. Steffen M.M., Belisle B.S., Watson S.B., Boyer G.L. & Wilhelm S.W. (2014) Status, causes and controls of cyanobacterial blooms in Lake Erie. Journal of Great Lakes Research, 40, 215-225.
48. Sverdrup H. (1953) On conditions for the vernal blooming of phytoplankton. Journal du Conseil, 18, 287-295.
49. 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.
50. Vanderploeg H.A., Liebig J.R., Nalepa T.F., Fahnenstiel G.L. & Pothoven S.A. (2010) Dreissena and the disappearance of the spring phytoplankton bloom in Lake Michigan. Journal of Great Lakes Research, 36, 50-59.
51. Vanderploeg H.A., Nalepa T.F., Jude D.J., Mills E.L., Holeck K.T., Liebig J.R. et al. (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.
52. Wang J., Bai X., Hu H., Clites A., Colton M. & Lofgren B. (2012) Temporal and spatial variability of great lakes ice cover, 1973-2010. Journal of Climate, 25, 1318-1329.
53. Yousef F., Kerfoot W.C., Shuchman R. & Fahnenstiel G. (2014) Bio-optical properties and primary production of Lake Michigan: insights from 13-years of SeaWiFS imagery. Journal of Great Lakes Research, 40, 317-324.
54. Zhou Y., Obenour D.R., Scavia D., Johengen T.H. & Michalak A.M. (2013) Spatial and temporal trends in Lake Erie hypoxia, 1987-2007. Environmental Science & Technology, 47, 899-905.
55. Zimmerman D.L. (2010) Likelihood-Based Methods. In: Handbook of Spatial Statistics. (Eds A.E. Gelfand, P.J.Diggle, M. Fuentes & P. Guttorp), pp. 45-56. CRC Press, Boca Raton, FL.