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Factors affecting fertilization success in two species of patellid limpet (Mollusca: Gastropoda) and development of fertilization kinetics models

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Abstract

Laboratory experiments were undertaken to examine fertilization success in the intertidal prosobranch limpets Patella ulyssiponensis and Patella vulgata. Alkalization of eggs (10 min in pH 9.0 sea water) prior to fertilization trials improved fertilization rates greatly. Fertilization success was found to be a function of sperm concentration, gamete age and contact time. Sperm concentration needed for optimum fertilization success in vivo ranged between 105 and 107 sperm ml−1 for both species although at higher concentrations the number of normally developing trochophore larvae decreased. For P. vulgata, sperm longevity (at a concentration of 106 sperm ml−1) did not exceed 6 h, whereas eggs of both species were fertilizable for up to 12 h. Maximum fertilization success occurred after 15–30 min gamete contact time. The Vogel et al. (Math Biosci 58:189–216, 1982) fertilization kinetics model is developed to allow for non-complete fertilizations under optimal sperm concentrations, and a new parameter fitting technique is developed to improve estimates of fertilization success for short gamete contact times.

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References

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

    Article  Google Scholar 

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

    Article  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  CAS  Google Scholar 

  • Baker MC (2001) Fertilization kinetics in marine invertebrates. University of Southampton Faculty of Science School of Ocean and Earth Sciences, PhD Thesis, 173 pp

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

    Article  Google Scholar 

  • Belding DL (1910) A report on the scallop fishery of Massachusetts; including the habits, life history of Pecten irradians, its rate of growth and other facts of economic value. Special Report, Commissioners on Fisheries and Game, Boston, 150 pp

  • 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  CAS  Google Scholar 

  • Bolton TF, Havenhand JN (1996) Chemical mediation of sperm activity and longevity in the solitary ascidians Ciona intestinalis and Ascidiella aspersa. Biol Bull 190:329–335

    Article  CAS  Google Scholar 

  • Bouch PJ, Olive PJW (2005) Impact of pH on oocyte fertilization and overrun of meiotic checkpoints leading to parthenogenetic development in Nereis virens. Invertebr Reprod Dev 48:1–5

    Article  Google Scholar 

  • Bowman RS (1985) The biology of the limpet Patella vulgata L. in the British Isles: spawning time as a factor determining recruitment success. In: Moore PG, Seed R (eds) The ecology of rocky shore coasts. Hodder and Stroughton Press, London, pp 178–193

    Google Scholar 

  • Branch GM, Odendaal F (2003) The effects of marine protected areas on the population dynamics of a South African limpet, Cymbula oculus, relative to the influence of wave action. Biol Conserv 114:255–269

    Article  Google Scholar 

  • Chia F-S, Bickell LR (1983) Spermatogenesis and sperm function. In: Adiyodi KG, Adiyodi RG (eds) Echinodermata. Reproductive Biology of Invertebrates, vol 2. Wiley, New York, pp 545–620

  • Claereboudt M (1999) Fertilization success in spatially distributed populations of benthic free-spawners: a simulation model. Ecol Model 121:221–233

    Article  Google Scholar 

  • Clavier J (1992) Fecundity and optimal sperm density for fertilization in the ormer (Haliotis tuberculata). In: Shepherd SA, Tegner MJ, Guzman Del Proo SA (eds) Abalone of the world: biology, fisheries and culture. Blackwell Scientific Publications, Oxford, pp 86–92

    Google Scholar 

  • Clotteau G, Dubé F (1993) Optimization of fertilization parameters for rearing surf clams (Spisula solidissima). Aquaculture 114:339–353

    Article  Google Scholar 

  • Damen P, Dictus WJAG (1994) Cell lineage of the prototroch of Patella vulgata (Gastropoda, Mollusca). Dev Biol 162:364–383

    Article  CAS  Google Scholar 

  • Deguchi R, Osani K (1994a) Repetitive intracellular Ca2+ increases at fertilization and the role of Ca2+ in meiosis reinitiation from the first metaphase in oocytes of marine bivalves. Dev Biol 163:162–174

    Article  CAS  Google Scholar 

  • Deguchi R, Osani K (1994b) Meiosis reinitiation from the first prophase is dependent on the levels of intracellular Ca2+ and pH in oocytes of the bivalves Mactra chinensis and Limaria hakodatensis. Dev Biol 166:587–599

    Article  CAS  Google Scholar 

  • Denny MW (1987) Life in the maelstrom: the biomechanics of wave-swept rocky shores. TREE 2(3):61–66

    CAS  PubMed  Google Scholar 

  • Denny MW, Shibata MF (1989) Consequences of surf-zone turbulence for settlement and external fertilization. Am Nat 134(6):859–889

    Article  Google Scholar 

  • Denny MW, Dairiki J, Distefano S (1992) Biological consequences of topography on wave-swept rocky shores: I. Enhancement of fertilisation. Biol Bull 183:220–232

    Article  CAS  Google Scholar 

  • Denny MW, Nelson EK, Mead KS (2002) Revised estimates of the effects of turbulence on fertilisation in the purple sea urchin Strongylocentrotus purpuratus. Biol Bull 203:275–277

    Article  Google Scholar 

  • Dodd JM (1955) Artificial fertilization, larval development and metamorphosis in Patella vulgata L. and Patella coerulea L. Pubbl Staz Napoli 29:172–186

    Google Scholar 

  • Encena VC II, Capinpin EC Jr, Bayona NC (1998) Optimal sperm concentration and time for fertilization of the tropical abalone, Haliotis asinina Linne 1758. Aquaculture 165:347–352

    Article  Google Scholar 

  • Gao X, Liu YF, Liu YX, Lin J (1990) The effect of sperm density of abalone on the egg fertilization rate and the abnormal rate of fertilized eggs. Trans Oceanol Limnol 3:71–75

    Google Scholar 

  • Gascoigne J, Lipcius RN (2004) Allee effects in marine systems. Mar Ecol Prog Ser 269:49–59

    Article  Google Scholar 

  • Gould MC, Stephano JL, Ortiz-Barron BJ, Perez-Quezada I (2001) Maturation and fertilization in Lottia gigantea oocytes: intracellular pH, Ca2+, and electrophysiology. J Exp Zool 290:411–420

    Article  CAS  Google Scholar 

  • Gross F, Smyth JC (1946) The decline of oyster populations. Nature 157:540–542

    Article  Google Scholar 

  • Guerrier P, Guerrier C, Neant I, Moreau M (1986) Germinal vesicle nucleoplasm and intracellular pH requirements for cytoplasmic maturity in oocytes of the prosobranch mollusk Patella vulgata. Dev Biol 116:92–99

    Article  Google Scholar 

  • Havenhand JN (1991) Fertilization and the potential for dispersal of gametes and larvae in the solitary ascidian Ascidia mentula Müller. Ophelia 33(1):1–15

    Article  Google Scholar 

  • Hawkins SJ, Corte-Real HBSM, Pannacciulli FG, Webber LC, Bishop JDD (2000) Thoughts on the ecology and evolution of intertidal biota of the Azores and other Atlantic islands. Hydrobiologia 440:3–17

    Article  Google Scholar 

  • Jantzen TM, de Nys R, Havenhand JN (2001) Fertilisation success and the effects of sperm chemoattractants on effective egg size in marine invertebrates. Mar Biol 138:1153–1161

    Article  Google Scholar 

  • Le Quesne WJF (2005) The response of a protandrous species to exploitation, and the implications for management: a case study with patellid limpets. University of Southampton, Faculty of Science, School of Ocean and Earth Sciences, PhD Thesis, 202 pp

  • Levitan DR (1995) The ecology of fertilization in free-spawning invertebrates. In: McEdward LR (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 123–156

  • Levitan DR, Sewell MA (1998) Fertilization success in free-spawning marine invertebrates: a review of the evidence and fisheries implications. Can Spec Publ Fish Aquat Sci 125:159–164

    Google Scholar 

  • Levitan DR, Young CM (1995) Reproductive success in large populations: empirical measures and theoretical predictions of fertilisation 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  CAS  Google Scholar 

  • Lewis DM, Pedley TJ (2001) The influence of turbulence on plankton predation strategies. J Theor Biol 210:347–365

    Article  CAS  Google Scholar 

  • Lundquist CJ, Botsford LW (2004) Model projections on the implications of the Allee effect in broadcast spawners. Ecol Appl 14:929–941

    Article  Google Scholar 

  • Luttikhuizen PC, Honkoop PJC, Drent J, van der Meer J (2004) A general solution for optimal egg size during external fertilization, extended scope for intermediate optimal egg size and the introduction of Don Ottavio ‘tango’. J Theor Biol 231:333–343

    Article  CAS  Google Scholar 

  • Marshall DJ, Styan CA, Keough MJ (2000) Intraspecific co-variation between egg and body size affects fertilization kinetics of free-spawning marine invertebrates. Mar Ecol Prog Ser 195:305–309

    Article  Google Scholar 

  • Martins HR, Santos RS, Hawkins SJ (1987) Exploitation of limpets (Patella spp.) in the Azores with a preliminary analysis of the stocks. ICES Report 1987/K 53:1–17

    Google Scholar 

  • Mead KS, Denny MW (1995) The effects of hydrodynamic shear stress on fertilization and early development of the purple sea urchin Strongylocentrotus purpuratus. Biol Bull 188:46–56

    Article  CAS  Google Scholar 

  • Meidel SK, Scheibling RE (2001) Variation in egg spawning among subpopulations of sea urchins Strongylocentrotus droebachiensis: a theoretical approach. Mar Ecol Prog Ser 213:97–110

    Article  Google Scholar 

  • Metaxas A, Scheibling RE, Young CM (2002) Estimating fertilization success in marine benthic invertebrates: a case study with the tropical sea star Oreaster reticulatus. Mar Ecol Prog Ser 226:87–101

    Article  Google Scholar 

  • Mill TS, McCormick TB (1992) Optimum sperm density for fertilization in three species of abalone (Haliotis). In: Shepherd SA, Tegnor MG, Guzman del Proo SA (eds) Abalone of the world. Biology, fisheries and culture. Blackwell Scientific Publications, London, pp 42–48

    Google Scholar 

  • Miller RB, Andersen MJ (2003) The kinetics of monospermic and polyspermic fertilization in free-spawning marine invertebrates. J Theor Biol 224:79–85

    Article  Google Scholar 

  • Orton JH, Southward AJ, Dodd JM (1956) Studies on the biology of limpets. II. The breeding of Patella vulgata L. in Britain. J Mar Biol Assoc UK 35:149–176

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Powell DK, Tyler PA, Peck LS (2001) Effect of sperm concentration and sperm ageing on fertilisation success in the Antarctic soft-shelled clam Laternula elliptica and the Antarctic limpet Nacella concinna. Mar Ecol Prog Ser 215:191–200

    Article  Google Scholar 

  • Quinn JF, Wing SR, Botsford LW (1993) Harvest refugia in marine invertebrate fisheries: models and applications to the red sea urchin, Strongylocentrotus franciscanus. Am Zool 33:537–550

    Article  Google Scholar 

  • Roberts CM, Hawkins JP (1999) Extinction risk in the sea. TREE 14(6):241–246

    CAS  PubMed  Google Scholar 

  • Rothschild BJ, Osborn TR (1988) Small-scale turbulence and plankton contact rates. J Plankton Res 10:465–474

    Article  Google Scholar 

  • Serrao EA, Pearson G, Kautsky L, Brawley SH (1996) Successful external fertilisation in turbulent environments. Proc Natl Acad Sci USA 93:5286–5290

    Article  CAS  Google Scholar 

  • Smith FGW (1935) The development of Patella vulgata. Philos Trans R Soc Lond Ser B 225:95–125

    Article  Google Scholar 

  • Styan CA (1998) Polyspermy, egg size, and the fertilization kinetics of free-spawning marine invertebrates. Am Nat 152:290–297

    CAS  PubMed  Google Scholar 

  • Styan CA, Butler AJ (2000) Fitting fertilisation kinetics models for free spawning marine invertebrates. Mar Biol 137:943–951

    Article  Google Scholar 

  • Van den Biggelaar JAM (1977) Development of dorsoventral polarity and mesentoblast determination in Patella vulgata. J Morphol 154:157–186

    Article  Google Scholar 

  • Vogel H, Czihak G, Chang P, Wolf W (1982) Fertilization kinetics of sea urchin eggs. Math Biosci 58:189–216

    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 

  • Wanninger A, Ruthensteiner B, Lobenwein S, Salvenmoser W, Dictus WJAG, Haszprunar G (1999) Development of the musculature in the limpet Patella (Mollusca, Patellogastropoda). Dev Genes Evol 209:226–238

    Article  CAS  Google Scholar 

  • Weber LI, Hawkins SJ (2005) Patella aspera and P. ulyssiponensis: genetic evidence of speciation in the North-east Atlantic. Mar Biol 147:153–162

    Article  Google Scholar 

  • Williams ME, Bentley MG (2002) Fertilisation success in marine invertebrates: the influence of gamete age. Biol Bull 202:34–42

    Article  Google Scholar 

  • Williams ME, Bentley MG, Hardedge JD (1997) Assessment of field fertilization success in the infaunal polychaete Arenicola marina (L.). Invertebr Reprod Dev 31:189–197

    Article  Google Scholar 

  • Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? TREE 15(1):10–13

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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Acknowledgements

This work was funded by grants to A.N.H. from the Royal Society (London) and National Research Foundation (South Africa). W.J.F. Le Q was funded by the N.E.R.C. at the N.O.C., Southampton. S.J.H. and J.D.D.B. were funded by N.E.R.C. grant-in-aid fellowships at the M.B.A. In addition the work at the M.B.A. was made possible by a Ray Lankester Fellowship to A.N.H. John Shepherd provided helpful comments on the model fitting, and Rosana Aquino Souza assisted with some of the experimental work on P. ulyssiponensis.

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  1. Will J. F. Le Quesne

    Present address: School of Marine Science and Technology, Newcastle University, Newcastle, UK

Authors and Affiliations

  1. Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa

    Alan N. Hodgson

  2. National Oceanography Centre, Waterfront Campus, University of Southampton, Southampton, SO14 3HZ, UK

    Will J. F. Le Quesne

  3. Marine Biological Association, Citadel Hill, Plymouth, PL1 2PB, UK

    Stephen J. Hawkins & John D. D. Bishop

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  1. Alan N. Hodgson
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  2. Will J. F. Le Quesne
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Correspondence to Alan N. Hodgson.

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Communicated by O. Kinne, Oldendorf/Luhe

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Hodgson, A.N., Le Quesne, W.J.F., Hawkins, S.J. et al. Factors affecting fertilization success in two species of patellid limpet (Mollusca: Gastropoda) and development of fertilization kinetics models. Mar Biol 150, 415–426 (2007). https://doi.org/10.1007/s00227-006-0354-9

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