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Biological and ecological mechanisms for overcoming sperm limitation in invasive dreissenid mussels

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Abstract

Many broadcast-spawning benthic invertebrates are subject to sperm limitation yet achieve high population densities, as for example dreissenid mussels (Dreissena polymorpha and Dreisssena bugensis) that were introduced into the Laurentian Great Lakes. The question remains whether biological or ecological/physical mechanisms reduce sperm limitation. Gamete dilution/longevity experiments were undertaken to determine whether dreissenid mussels are subject to sperm limitation, and computational fluid dynamic modeling was used to determine the potential influence of bottom roughness on sperm dilution in nature. Results indicated that dreissenid mussels may be sperm limited, but the extent to which sperm dilution affects them is lower than what was reported for other broadcast spawning invertebrates. Importantly, model mussel clusters influenced external fertilization by retaining sperm in downstream eddies but allowing downstream transport from one cluster to another. This, in addition to high sperm potency at low sperm concentrations, may help to explain the success of dreissenid mussels as invasive species.

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References

  • Ackerman JD (2002) Diffusivity in a marine macrophyte bed: implications for submarine pollination and dispersal. Am J Bot 89:1119–1127

    Article  PubMed  Google Scholar 

  • Ackerman JD, Sim B, Nichols SJ, 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

    Article  Google Scholar 

  • Ackerman JD, Loewen MR, Hamblin PF (2001) Benthic-pelagic coupling over a zebra mussel reef in western Lake Erie. Limnol Oceanogr 46:892–904

    Article  Google Scholar 

  • André C, Lindegarth M (1995) Fertilization efficiency and gamete viability of a sessile, free-spawning bivalve, Cerastoderma edule. Ophelia 43:215–227

    Article  Google Scholar 

  • Babcock R, Kessing J (1999) Fertilization biology of the abalone Haliotis laevigata: laboratory and field studies. Can J Fish Aquat Sci 56:1668–1678

    Google Scholar 

  • Babcock RC, Mundy CN, Whitehead D (1994) Sperm diffusion models and in situ confirmation of long-distance fertilization in the free-spawning asteroid Acanthaster planci. Biol Bull 186:17–28

    Article  Google Scholar 

  • Baker MC, Tyler PA (2001) Fertilization success in the commercial gastropod Haliotis tuberculata. Mar Ecol Prog Ser 211:205–213

    Article  Google Scholar 

  • Benzie JAH, Dixon P (1994) The effects of sperm concentration, sperm:egg ratio, and gamete age on fertilization success in crown-of-thorns starfish (Acanthaster planci) in the laboratory. Biol Bull 186:139–152

    Article  Google Scholar 

  • Bishop JDD (1998) Fertilization in the sea: are the hazards of broadcast spawning avoided when free-spawned sperm fertilize retained eggs? Proc R Soc Lond B 265:725–731

    Article  Google Scholar 

  • Brady VJ, Cardinale BJ, Burton TM (1995) Zebra mussels in a costal marsh: the seasonal and spatial limits of colonization. J Great Lakes Res 21:587–593

    Article  Google Scholar 

  • Chang ER, Veeneklass RM, Buitenwerf R, Bakker JP, Bouma TJ (2008) To move or not to move: determinants of seed retention in a tidal marsh. Funct Ecol 22:720–727

    Article  Google Scholar 

  • Ciereszko A, Dabrowski K, Piros B, Kwasnik M, Glogowski J (2001) Characterization of zebra mussel (Dreissena polymorpha) sperm motility: duration of movement, effects of cations, pH and gossypol. Hydrobiologia 452:225–232

    Article  CAS  Google Scholar 

  • Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141

    Article  Google Scholar 

  • Denny MW, Shibata M (1989) Consequences of surf-zone turbulence for settlement and fertilization. Am Nat 134:859–889

    Article  Google Scholar 

  • Devin S, Beisel JN (2007) Biological and ecological characteristics of invasive species: a gammarid study. Biol Invasions 9:13–24

    Article  Google Scholar 

  • Dong Y, Yao H, Lin Z, Zhu D (2011) The effects of sperm–egg ratios on polyspermy in the blood clam, Tegillarca granosa. Aquacult Res 42. doi:10.1111/j.1365-2109.2011.02799.x

  • Fallis LC, Stein KK, Lynn JW, Misamore MJ (2010) Identification and role of carbohydrates on the surface of gametes in the zebra mussel, Dreissena polymorpha. Biol Bull 218:61–74

    PubMed  CAS  Google Scholar 

  • Hardege JD, Ram JL, Bentley MG (1997) Activation of spawning in zebra mussels by algae-, cryptomonad-, and gamete-associated factors. Exp Biol Online 2:2

    Google Scholar 

  • Hebert PDN, Muncaster BW, Mackie GL (1989) Ecological and genetic studies on Dreissena polymorpha (Pallas): a new mollusc in the Great Lakes. Can J Fish Aquat Sci 46:1587–1591

    Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Inamdar MV, Kim T, Chung Y-K, Was AM, Xiang X, Wang C-W, Takayama S, Lastoskie CM, Thomas FIM, Sastry AM (2007) Assessment of sperm chemokinesis with exposure to jelly coats of sea urchin eggs and resact: a microfluidic experiment and numerical study. J Exp Biol 210:3805–3820

    Article  PubMed  CAS  Google Scholar 

  • Lamare MD, Stewart BG (1998) Mass spawning by the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord. Mar Biol 132:135–140

    Article  Google Scholar 

  • Levitan DR (1993) The importance of sperm limitation to the evolution of egg size in marine invertebrates. Am Nat 141:517–536

    Article  PubMed  CAS  Google Scholar 

  • Levitan DR (2005) Sex-specific spawning behavior and its consequences in an external fertilizer. Am Nat 165:682–694

    Article  PubMed  Google Scholar 

  • Levitan DR, Young CM (1995) Reproductive success in large populations: empirical measures and theoretical predictions of fertilization in the sea biscuit Clypeaster rosaceus. J Exp Mar Biol Ecol 190:221–241

    Article  Google Scholar 

  • Levitan DR, Sewell MA, Chia F-S (1991) Kinetics of fertilization in the sea urchin Strongylocentrotus franciscanus: interaction of gamete dilution, age, and contact time. Biol Bull 181:371–378

    Article  Google Scholar 

  • Loewen MR, Ackerman JD, Hamblin PF (2007) Environmental implications of stratification and turbulent mixing in a shallow lake basin. Can J Fish Aquat Sci 64:43–57

    Article  CAS  Google Scholar 

  • Luetjens CM, Dorresteijn AWC (1995) Multiple, alternative cleavage patterns precede uniform larval morphology during normal development of Dreissena polymorpha (Mollusca, Lamellibranchia). Roux’s Arch Dev Biol 205:138–149

    Article  Google Scholar 

  • Manriquez PH, Hughes RN, Bishop JDD (2001) Age-dependent loss of fertility in water-borne sperm of the bryozoan Celleporella hyaline. Mar Ecol Prog Ser 224:87–92

    Article  Google Scholar 

  • Marsden JE, Lansky DM (2000) Substrate selection by settling zebra mussels, Dreissena polymorpha, relative to material, texture, orientation, and sunlight. Can J Zool 78:787–793

    Google Scholar 

  • Marshall DJ, Bolton TF (2007) Sperm release strategies in marine broadcast spawners: the costs of releasing sperm quickly. J Exp Biol 210:3720–3727

    Article  PubMed  Google Scholar 

  • Marshall DJ, Semmens D, Cook C (2004) Consequences of spawning at low tide: limited gamete dispersal for a rockpool anemone. Mar Ecol Prog Ser 266:135–142

    Article  Google Scholar 

  • McNichols KA, Mackie GL, Ackerman JD (2011) Host fish quality may explain the status of endangered Epioblasma torulosa rangiana and Lampsilis fasciola (Bivalvia: Unionidae) in Canada. J N Am Benthol Soc 30:60–70

    Article  Google Scholar 

  • Miller RL, Mojares JJ, Ram JL (1994) Species-specific sperm attraction in the zebra mussel, Dreissena polymorpha, and the quagga mussel, Dreissena bugensis. Can J Zool 72:1764–1770

    Article  Google Scholar 

  • Misamore MJ, Lynn JW (2000) Role of cytoskeleton in sperm entry during fertilization in the freshwater bivalve Dreissena polymorpha. Biol Bull 199:144–156

    Article  PubMed  CAS  Google Scholar 

  • Misamore M, Silverman H, Lynn JW (1996) Analysis of fertilization and polyspermy in serotonin-spawned eggs of the zebra mussel, Dreissena polymorpha. Mol Reprod Dev 43:205–216

    Article  PubMed  CAS  Google Scholar 

  • Nichols SJ, Black MG (1994) Identification of larvae: the zebra mussel (Dreissena Polymorpha), quagga mussel (Dreissena rosteriformis bugensis), and Asian clam (Corbicula fluminea). Can J Zool 72:406–417

    Article  Google Scholar 

  • Oliver J, Babcock R (1992) Aspects of the fertilization ecology of broadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. Biol Bull 183:409–417

    Article  Google Scholar 

  • Pearson GA, Serrao EA, Brawley SH (1998) Control of gamete release in flucoid algae: sensing hydrodynamic conditions via carbon acquisition. Ecology 79:1725–1739

    Article  Google Scholar 

  • Pennington JT (1985) The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169:417–430

    Article  Google Scholar 

  • Ram JL, Palazzo SM (2008) Globalization of an Aquatic Pest: Economic Costs, Ecological Outcomes, and Positive Applications of Zebra Mussel Invasions and Expansions. Geogr Compass 2:1755–1776

    Article  Google Scholar 

  • Ram JL, Crawford GW, Walker JU, Mojares JJ, Patel N, Fong PP, Kyozuka K (1993) Spawning in the zebra mussel (Dreissena polymorpha): activation by internal or external application of serotonin. J Exp Zool 265:587–598

    Article  PubMed  CAS  Google Scholar 

  • Reidel IH, Kruse K, Howard J (2005) A self-organized vortex array of hydrodynamically entrained sperm cells. Science 309:300–303

    Article  Google Scholar 

  • Schindler RJ, Ackerman JD (2010) The environmental hydraulics of turbulent boundary layers. In: Mihailovic DT, Gualtieri C (eds) Advances in Environmental Fluid Mechanics. World Scientific, London, pp 87–126

    Chapter  Google Scholar 

  • Sprung M (1993) The other life: an account of present knowledge of the larval phase of Dreissena polymorpha. In: Nalepa TF, Schloesser D (eds) Zebra mussels: biology, impacts, control. Lewis Publishers, Boca Raton, pp 39–53

    Google Scholar 

  • Stoeckel JA, Padilla DK, Schneider DW, Rehmann CR (2004) Laboratory culture of Dreissena polymorpha larvae; spawning success, adult fecundity, and larval mortality patterns. Can J Zool 82:1436–1443

    Article  Google Scholar 

  • Stoeckmann A (2003) Physiological energetics of Lake Erie dreissenid mussels: a basis for the displacement of Dreissena polymorpha by Dreissena bugensis. Can J Fish Aquat Sci 60:126–134

    Article  Google Scholar 

  • Styan CA, Kupriyanova E, Havenhand JN (2008) Barriers to cross-fertilization between populations of a widely dispersed polychaete species are unlikely to have arisen through gametic compatibility arms-races. Evol 62:3041–3055

    Article  Google Scholar 

  • Wahle RA, Peckham SH (1999) Density-related reproductive trade-offs in the green sea urchin, Strongylocentrotus droebachiensis. Mar Biol 134:127–137

    Article  Google Scholar 

  • Wright DA, Setzler-Hamilton EM, Magee JA, Kennedy VS, McIninch SP (1996) Effect of salinity and temperature on survival and development of young zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussels. Estuaries 19:619–628

    Article  Google Scholar 

  • Yund PO, Meidel SK (2003) Sea urchin spawning in the benthic boundary layer: are eggs fertilized before advecting away from females? Limnol Oceanogr 48:795–801

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. G. Nishihara, P. Ragaz, K. McNichols, and B. Hunt for their assistance in the laboratory and field. We also thank several anonymous reviews for their comments on an earlier draft. This work was funded by a NSERC Discovery Grant to JDA.

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Correspondence to Josef D. Ackerman.

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Quinn, N.P., Ackerman, J.D. Biological and ecological mechanisms for overcoming sperm limitation in invasive dreissenid mussels. Aquat Sci 74, 415–425 (2012). https://doi.org/10.1007/s00027-011-0237-0

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