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Sperm motility and longevity in the giant cuttlefish, Sepia apama (Mollusca: Cephalopoda)

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Abstract

The sperm kinetics and fertilisation literature in marine invertebrates is heavily biased toward free-spawning species. Nonetheless, many species (e.g. cephalopods) transfer and/or fertilise gametes in confined external spaces or internally, creating very different selective pressures on sperm storage, sperm longevity and hence sperm competition. Here we report the results of an investigation into the effects of sperm age, water temperature and sperm concentration on sperm motility in the giant cuttlefish (Sepia apama). Significant positive correlations were found between percent motility and sperm concentration, and between sperm motile speed and sperm concentration. Mean percent motility of cuttlefish sperm suspension was still 9% eight hours after being released from the spermatophore and diluted into filtered seawater at 12°C (ambient field temperature during the spawning season). Sperm resuspended from spermatangia taken from (mated) females in the field were motile for up to 100 hours. When spermatophores were stored at 4°C motility was still observed in resuspended sperm after two months. Our results show that spermatangia and spermatophores can retain and release live sperm for long periods. The observed longevity of sperm in S. apama greatly increases the potential for sperm competition in this species.

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References

  • Au DWT, Lau CY, Chan KL, Wu RSS (2001) Reproductive impairment of sea urchins upon chronic exposure to cadmium Part I: Effects on gamete quality. Env Poll 111:1–9

    Article  CAS  Google Scholar 

  • Austin CR, Lutwark-Mann C, Mann T (1964) Spermatophores and spermatozoa of the squid Loligo pealii. Proc R Soc Lond B 161:143–152

    Article  CAS  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  CAS  Google Scholar 

  • Birkhead T, Møller AP (1992) Sperm Competition in Birds: Evolutionary Causes and Consequences. Academic Press, London

    Google Scholar 

  • Birkhead T, Møller AP (1998) Sperm Competition and Sexual Selection. Academic Press, London

    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 

  • 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 

  • Buskey EJ, Lenz PH, Hartline DK (2002) Escape behavior of planktonic copepods in response to hydrodynamic disturbances: high speed video analysis. Mar Ecol Prog Ser 235:135–146

    Article  Google Scholar 

  • Chia F-S, Bickell LR (1983) Echinodermata. In: Adiyodi KG, Adiyodi RG (eds) Reproductive Biology of Invertebrates, Volume II: Spermatogenesis and Sperm Function. John Wiley, New York, pp. 545–620

  • Coma R, Lasker HR (1997) Effects of spatial distribution and reproductive biology on in situ fertilization rates of a broadcast-spawning invertebrate. Biol Bull 193:20–29

    Article  CAS  Google Scholar 

  • Eberhard WG (1996) Female Control: Sexual Selection by Cryptic Female Choice. Princeton University Press, Princeton

    Google Scholar 

  • Farley GS (2002) Helical nature of sperm swimming affects the fit of fertilization-kinetics models to empirical data. Biol Bull 203:51–57

    Article  Google Scholar 

  • Geffen AJ (1999) Variations in sperm motility of the Atlantic herring Clupea harengus. Mar Biol 134:637–643

    Article  Google Scholar 

  • Hall KC, Hanlon RT (2002) Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140:533–545

    Article  Google Scholar 

  • Hanlon RT, Messenger JB (1996) Cephalopod Behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Hanlon RT, Ament SA, Gabr H (1999) Behavioral aspects of sperm competition in cuttlefish, Sepia officinalis (Sepioidea: Cephalopoda). Mar Biol 134:719–728

    Article  Google Scholar 

  • Iken K, Greer SP, Amsler CD, McClintock JB (2003) A new antifouling bioassay monitoring brown algal spore swimming behaviour in the presence of echinoderm extracts. Biofouling 19:327–334

    Article  Google Scholar 

  • Johnson SL, Yund PO (2004) Remarkable longevity of dilute sperm in a free-spawning colonial ascidian. Biol. Bull. 206:144–151

    Article  Google Scholar 

  • Kupriyanova E, Havenhand JN (2002) Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa Invertebr. Repro Dev 41:21–2

    Google Scholar 

  • Levitan DR (1993) The importance of sperm limitation to the evolution of egg size in marine invertebrates. Am Nat 14:517–536

    Article  Google Scholar 

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

    Google Scholar 

  • Levitan DR (1996) Effects of gamete traits on the fertilization in the sea and the evolution of sexual dimorphism. Nature 382:153–155

    Article  CAS  Google Scholar 

  • Levitan DR (2000) Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc R Soc Lond B 267:531–534

    Article  CAS  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 

  • Lillie FR (1915) Studies of fertilization. VII. Analysis of variations in the fertilization power of pserm suspensions of Arbacia. Biol Bull 28:229–251

    Article  Google Scholar 

  • Lopez-de-Victoria G, Zimmer-Faust RK, Lovell CR (1995) Computer-assisted video motion analysis: A powerful technique for investigating motility and chemotaxis. J. Microb. Methods 23:329–341

    Article  Google Scholar 

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

    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 

  • Miller RL (1975) Chemotaxtis in the spermatozoa of Ciona intestinalis. Nature 254:244–245

    Article  CAS  Google Scholar 

  • Naud M-J, Hanlon RT, Hall KC, Shaw PW, Havenhand JN (2004) Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. An Behav 67:1043–1050

    Article  Google Scholar 

  • Naud M-J, Shaw PW, Hanlon RT, Havenhand JN (2005) Evidence for biased use of sperm sources in wild female giant cuttlefish (Sepia apama). Proc R Soc Lond B 272:1047–1051

    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  CAS  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead T, Møller AP (eds) Sperm Competition and Sexual Selection. Academic Press, London

    Google Scholar 

  • Pearse DE, Janzen FJ, Avise JC (2002) Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behav Ecol Sociobiol 51:164–171

    Article  Google Scholar 

  • Prosser CL (1991) Temperature. In: Prosser CL (eds) Environmental and Metabolic Animal Physiology. Willey-Liss Inc, New-York, pp 109–165

    Google Scholar 

  • Riffell JA, Krug PJ, Zimmer RK (2002) Fertilization in the sea: the chemical identity of an abalone sperm attractant. J Exp Biol 205:1439–145

    CAS  PubMed  Google Scholar 

  • Simmons LW, Siva-Jothy MT (1998) Sperm competition in insects: mechanisms and the potential for selection. In: Birkhead T, Møller AP (eds) Sperm Competition and Sexual Selection. Academic Press, London

    Google Scholar 

  • Siva-Jothy MT (1987) The structure and function of the female sperm-storage organs in libellulid dragonflies. Journal of insect physiology 33:559–567

    Article  Google Scholar 

  • Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: The evolution of testis size and ejaculate characteristics. Am Nat 149:933–954

    Article  CAS  Google Scholar 

  • Strathmann M (1987) Distribution and Development of Marine Invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle

    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 

  • Tamburri MN, Zimmer-Faust RK, Tamplin ML (1992) Natural sources and properties of chemical inducers mediating settlement of oyster larvae - a reexamination. Biol Bull 183:327–338

    Article  CAS  Google Scholar 

  • Trippel EA, Morgan MJ (1994) Sperm longevity in Atlantic cod (Gadus morhua). Copeia 4:1025–1029

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Yund PO (1990) An insitu measurement of sperm dispersal in a colonial marine hydroid. J Exp Zool 253:102–106

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank T. Jantzen, A. Hirst, and T. Bramley for most excellent assistance during the field operation, and special thanks to K. Hall and R. Hanlon for guidance and discussion. This study was supported by a grant from the Australian Research Council (to JNH), and a FCAR doctoral scholarship (to M-JN). The work described in this manuscript was conducted in accordance with state and national laws in Australia.

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Correspondence to Marie-José Naud.

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Communicated by J.P. Thorpe, Port Erin

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Naud, MJ., Havenhand, J.N. Sperm motility and longevity in the giant cuttlefish, Sepia apama (Mollusca: Cephalopoda). Marine Biology 148, 559–566 (2006). https://doi.org/10.1007/s00227-005-0109-z

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