Dreissenid (quagga and zebra mussel) veligers are adversely affected by bloom forming cyanobacteria (original) (raw)

Abstract

Quagga (Dreissena rostriformis bugensis) and zebra (D. polymorpha) mussels are broadcast spawners that produce planktonic, free swimming veligers, a life history strategy dissimilar to native North American freshwater bivalves. Dreissenid veligers require highly nutritious food to grow and survive, and thus may be susceptible to increased mortality rates during harsh environmental conditions like cyanobacteria blooms. However, the impact of cyanobacteria and one of the toxins they can produce (microcystin) has not been evaluated in dreissenid veligers. Therefore, we exposed dreissenid veligers to eleven distinct cultures (isolates) of cyanobacteria representing Anabaena, Aphanizomenon, Dolichospermum, Microcystis, and Planktothrix species and the cyanotoxin microcystin to determine the lethality of cyanobacteria on dreissenid veligers. Six-day laboratory bioassays were performed in microplates using dreissenid veligers collected from the Detroit River, Michigan, USA. Veligers were exposed to increasing concentrations of cyanobacteria and microcystin using the green algae Chlorella minutissima as a control. Based on dose response curves formulated from a Probit model, the LC 50 values for cyanobacteria used in this study range between 15.06 and 135.06 μg/L chlorophyll-a, with the LC 50 for microcystin-LR at 13.03 μg/L. Because LC 50 values were within ranges observed in natural waterbodies, it is possible that dreissenid recruitment may be suppressed when veliger abundances overlap with seasonal cyanobacteria blooms. Thus, the toxicity of cyanobacteria to dreissenid veligers may be useful to include in models forecasting dreissenid mussel abundance and spread.

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (44)

  1. Ackerman, J.D., Sim, B., Nichols, S.J., Claudi, R., 1994. A review of the early life history of zebra mussels (Dreissena polymorpha): comparisons with marine bivalves. Can. J. Zool. 72, 1169-1179.
  2. Basen, T., Martin-Creuzburg, D., Rothhaupt, K.O., 2011. Role of essential lipids in de- termining food quality for the invasive freshwater clam Corbicula fluminea. J. North Am. Benthol. Soc. 30, 653-664.
  3. Biggs, B.J.F., Kilroy, C., 2000. Stream Periphyton Monitoring Manual. National Institute of Water and Atmospheric Research (NIWA), Christchurch, New Zealand.
  4. Boegehold, A.G., Johnson, N.S., Ram, J.L., Kashian, D.R., 2018. Cyanobacteria reduce quagga mussel (Dreissena rostriformis bugensis) spawning and fertilization success. Freshw. Sci. 37, 510-518.
  5. Boltovskoy, D., Correa, N., Bordet, F., Leites, V., Cataldo, D., 2013. Toxic Microcystis (cyanobacteria) inhibit recruitment of the bloom-enhancing invasive bivalve Limnoperna fortunei. Freshw. Biol. 58, 1968-1981.
  6. Bowen, K.L., Conway, A.J., 2018. Could dreissenid veligers be the lost biomass of invaded lakes? Freshwater Science 37, 315-329.
  7. Carmichael, W., 1994. The toxins of cyanobacteria. Sci. Am. 270, 78-86.
  8. Carmichael, W.W., Boyer, G.L., 2016. Health impacts from cyanobacteria harmful algae blooms: implications for the North American Great Lakes. Harmful Algae 54, 194-212.
  9. Clearwater, S.J., Wood, S.A., Phillips, N.R., Parkyn, S.M., Van Ginkel, R., Thompson, K.J., 2014. Toxicity thresholds for juveniles freshwater mussels Echyridella menziesii and crayfish Paranephrops planifrons, after acute or chronic exposure to Microcystis sp. Environ. Toxicol. 29, 487-502.
  10. Dawson, R.M., 1998. The toxicology of microcystins. Toxicon 36, 953-962.
  11. Dionisio Pires, L.M., Kusserow, R., Van Donk, E., 2003. Influence of toxic and non-toxic phytoplankton on feeding and survival of Dreissena polymorpha (Pallas) larvae. Hydrobiologia 491, 193-200.
  12. Dionisio Pires, L.M., Karlsson, K.M., Meriluoto, J.A.O., Kardinaal, E., Visser, P.M., Siewertsen, K., Van Donk, E., Ibelings, B.W., 2004. Assimilation and depuration of microcystin-LR by the zebra mussel, Dreissena polymorpha. Aquat. Toxicol. 69, 385-396.
  13. Dyble, J., Fahnenstiel, G.L., Litaker, R.W., Millie, D.F., Tester, P.A., 2008. Microcystin concentration and genetic diversity of Microcystis in the lower Great Lakes. Environ. Toxicol. 23, 507-516.
  14. Guillard, R.R., Lorenzen, C.J., 1972. Yellow-green algae with chlorophylide c. J. Phycol. 8, 10-24.
  15. Harke, M.J., Steffen, M.M., Gobler, C.J., Otten, T.G., Wilhelm, S.W., Wood, S.A., Paerl, H.W., 2016. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium. Microcystis spp. Harmful Algae 54, 4-20.
  16. Huisman, J., Codd, G.A., Paerl, H.W., Ibelings, B.W., Verspagen, J.M.H., Visser, P.M., 2018. Cyanobacterial blooms. Nature Reviews Microbiology 16, 471-483.
  17. Johnson, L.E., 1995. Enhanced early detection and enumeration of zebra mussel (Dreissena spp.) veligers using cross-polarized microscopy. Hydrobiologia 312, 139-146.
  18. Juhel, G., Davenport, J., O'Halloran, J., Culloty, S., Ramsay, R., James, K., Furey, A., Allis, O., 2006. Pseudodiarrhoea in zebra mussels Dreissena polymorpha (Pallas) exposed to microcystins. J. Exp. Biol. 209, 810-816.
  19. Kennedy, A.J., Millward, R.N., Steevens, J.A., Lynn, J.W., Perry, K.D., 2006. Relative sensitivity of zebra mussel (Dreissena polymorpha) life-stages to two copper sources. J. Gt. Lakes Res. 32, 596-606.
  20. Lazareva, V.I., Kopylov, A.I., Sokolova, E.A., Pryanichnikova, E.G., 2016. Veliger larvae of dreissenids (Bivalvia, Dreissenidae) in the plankton foodweb of Rybinsk Reservoir. Biol. Bull. 43, 1313-1321.
  21. Liebig, J.R., Vanderploeg, H.A., 1995. Vulnerability of Dreissena polymorpha larvae to predation by Great Lakes calanoid copepods: the importance of the bivalve shell. J. Gt. Lakes Res. 21, 353-358.
  22. Liu, Y., Chen, W., Li, D., Huang, Z., Shen, Y., Liu, Y., 2010. Cyanobacteria-/cyanotoxin contaminations and eutrophication status before Wuxi drinking water crisis in Lake Taihu, China. J. Environ. Sci. 23, 575-581.
  23. Pacheco, A.G., de Freitas Rebelo, M., 2013. A simple R-based function to estimate lethal concentrations. Mar. Environ. Res. 91, 41-44.
  24. Quinn, N.P., Ackerman, J.D., 2012. Biological and ecological mechanisms for overcoming sperm limitation in invasive dreissenid mussels. Aquat. Sci. 74, 415-425.
  25. R Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria URL. https://www.R-project. org/.
  26. Ram, J.L., Karim, A.S., Acharya, P., Jagtap, P., Purohit, S., Kashian, D.R., 2011. Reproduction and genetic detection of veligers in changing Dreissena populations in the Great Lakes. Ecosphere 2, 1-16.
  27. Rastogi, R.P., R.P., Sinha, Incharoenskdi, A., 2014. The cyanotoxin-microcystins: current overview. Rev. Environ. Sci. Biotechnol. 13, 215-249.
  28. Sarnelle, O., White, J.D., Horst, G.G., Hamilton, S.K., 2012. Phosphorus addition reverses the positive effect of zebra mussels (Dreissena polymorpha) on the toxic cyano- bacterium, Microcystis aeruginosa. Water Res. 46, 3471-3478.
  29. Sayers, M., Fahnenstiel, G.L., Shuchman, R.A., Whitley, M., 2016. Cyanobacteria blooms in three eutrophic basins of the Great Lakes: a comparative analysis using satellite remote sensing. Int. J. Remote Sens. 37, 4148-4171.
  30. Sprung, M., 1991. Costs of reproduction: a study on metabolic requirements of the gonads and fecundity of the bivalve Dreissena polymorpha. Malacologia 33, 63-70.
  31. Stanczykowska, A., 1977. Ecology of Dreissena polymorpha (pall.) (bivalva) in lakes. Pol. Arch. Hydrobiol. 24, 461-530.
  32. Stewart-Malone, A., Misamore, M., Wilmoth, S., Reyes, A., Wong, W.H., Gross, J., 2015. The effect of UV-C exposure on larval survival of the dreissenid quagga mussel. PLoS One 10 (7). https://doi.org/10.137/journal.pone.0133039\. e0133039.
  33. Stoeckel, J.A., Padilla, D.K., Schneider, D.W., Rehmann, C.R., 2004. Laboratory culture of Dreissena polymorpha larvae: spawning success, adult fecundity, and larval mortality patterns. Can. J. Zool. 82, 1436-1443.
  34. Vanderploeg, H.A., Liebig, J.R., Gluck, A.A., 1996. Evaluation of different phytoplankton for supporting development of zebra mussel larvae (Dreissena polymorpha): the im- portance of size and polyunsaturated fatty acid content. J. Gt. Lakes Res. 22, 36-45.
  35. Vanderploeg, H.A., Liebig, J.R., Carmichael, W.W., Agy, M.A., Johengen, T.H., Fahnenstiel, G.L., Nalepa, T.F., 2001. Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in saginaw bay (Lake Huron) and Lake Erie. Can. J. Fish. Aquat. Sci. 58, 1208-1221.
  36. USEPA, 1991. Methods for Measuring the Acute Toxicity of Effluents and Receiving Waters to Freshwater and Marine Organisms. Environmental Monitoring Systems Laboratory, U. S. Environmental Protection Agency, Cincinnati, Ohio.
  37. Vanderploeg, H.A., Johengen, T.H., Liebig, J.R., 2009. Feedback between zebra mussel selective feeding and algal composition affects mussel condition: did the regime changer pay a price for its success? Freshw. Biol. 54, 47-63.
  38. Wacker, A.P., von Elert, E., 2002. Strong influences of larval diet history on subsequent post-settlement growth in the freshwater mollusc Dreissena polymorpha. Proc. Biol. Sci. 269, 2113-2119.
  39. Waller, D.L., Rach, J.J., Cope, W.G., Marking, L.L., 1993. Toxicity of candidate mollus- cicides to zebra mussels (Dreissena polymorpha) and selected nontarget organisms. J. Gt. Lakes Res. 19, 695-702.
  40. White, J.D., Sarnelle, O., 2014. Size-structured vulnerability of the colonial cyano- bacterium, Microcystis aeruginosa, to grazing by zebra mussels (Dreissena polymorpha). Freshw. Biol. 59, 514-525.
  41. Wright, D.A., Setzler-Hamilton, E.M., Magee, J.A., Harvey, H.R., 1996a. Laboratory cul- ture of zebra (Dreissena polymorpha) and quagga (D. bugensis) mussel larvae using estuarine algae. J. Gt. Lakes Res. 22, 46-54.
  42. Wright, D.A., Setzler-Hamilton, E.M., Magee, J.A., Kennedy, V.S., McIninch, S.P., 1996b. Effect of salinity and temperature on survival and development of young zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussels. Estuaries 19, 619-628.
  43. Wright, D.A., Magee, J.A., 1997. The toxicity of endod extract to the early life stages of Dreissena bugensis. Biofouling 11, 255-263.
  44. Yuan, L.L., Pollard, A.I., Pather, S., Oliver, J.L., D'Anglada, L., 2014. Managing micro- cystin: dentifying national-scale thresholds for total nitrogen and chlorophyll a. Freshw. Biol. 59, 1970-1981.