Advertisement

Marine Biology

, Volume 158, Issue 5, pp 1163–1173 | Cite as

Synchronous aggregated pseudo-copulation of the sea star Archaster angulatus Müller & Troschel, 1842 (Echinodermata: Asteroidea) and its reproductive cycle in south-western Australia

  • John K. Keesing
  • Fiona Graham
  • Tennille R. Irvine
  • Ryan Crossing
Original Paper

Abstract

Mass individual pairing or pseudo-copulation of the sea star Archaster angulatus was observed in November and December 2009, suggesting a late-spring/summer spawning period for this species on the west coast of Australia. Detailed measurements were made on the second of these occasions. Density of sea stars was 1.11 per m2 and 68.5% were in mating pairs. Copulating pairs were mostly male on female, occasionally male on male. There was no difference in size between males and females in mating pairs. No evidence was found to indicate mating and spawning is coincident with lunar or tidal cycles. Females outnumbered males by more than 20%, but the difference in sex ratio was not statistically significant. Analysis of the reproductive cycle revealed that gonad indices reached their peak in October and declined from then until January. Histological sections of gonads confirmed that sea stars are in peak reproductive condition in October and November and are fully spent by January. Males have a much lower (ca. 1/3rd) gonad index than females when each are in peak reproductive condition, the second lowest recorded for any sea star. Pyloric caecae indices showed little annual variation and monthly averages of just 3–4% are among the lowest ever recorded for an asteroid. It is suggested that these characteristics are associated with the copulatory behaviour of the deposit feeding A. angulatus, enabling the species to maintain a high level of fertilisation success while also minimising the allocation of energy to gonad development in habitats with low or variable food availability. However, it is still difficult to explain why a species which ensures a high level of fertilisation by pseudo-copulation also does this en masse and synchronously. One hypothesis is that competition for males and the benefits of having eggs fertilised by multiple males favours both synchrony and aggregation.

Keywords

Gonad Development Isotope Ratio Mass Spectrometry Mating Pair Gonad Index Multiple Male 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Professor John Lawrence, University of South Florida and Professor Dongyan Liu, Chinese Academy of Sciences for their advice, encouragement and comments on the manuscript. We also thank Sharon Yeo, Murdoch University for providing the monthly samples of sea stars, Jeremy Allen and Kim Elliot, Western Australian Department of Agriculture for preparing the histological mounts and two anonymous reviewers for helpful suggestions which improved the manuscript. This research was supported by funding from the Western Australian Marine Science Institution.

References

  1. Babcock R, Mundy C, Keesing J, Oliver J (1994) Predictable and un-predictable spawning events: in situ behavioural data from free spawning coral reef invertebrates. Invert Reprod Dev 22:213–219CrossRefGoogle Scholar
  2. Bosch I, Slattery M (1999) Costs of extended brood protection in the Antarctic sea star, Neosmilaster georgianus. Mar Biol 134:449–459CrossRefGoogle Scholar
  3. Boschma H (1924) Űber einen Fall von Kopulation bei einer Asteridae (Archaster typicus). Zool Anz 58:283–285Google Scholar
  4. Chia F-S, Atwood D, Crawford B (1975) Comparative morphology of echinoderm sperm and possible phylogenetic implications. Amer Zool 15:533–565Google Scholar
  5. Clark AM, Rowe FWE (1971) Monograph of shallow-water Indo-West Pacific echinoderms: i–vii, 1–238, pls 1–31. Trustees of the British Museum (Natural History), LondonGoogle Scholar
  6. Clemente LS, Anicete BZ (1949) Studies on sex-ratio, sexual dimorphism and early development of the common sea star, Archaster typicus Müller and Troschel (Family Archasteridae. Med Appl Sci Bull 9:297–318Google Scholar
  7. Forehead HI, Thompson PA (2010) Microbial communities of subtidal shallow sandy sediments change with depth and wave disturbance, but nutrient exchanges remain similar. Mar Ecol Prog Ser 414:11–26CrossRefGoogle Scholar
  8. Hamel J-F, Mercier A (1995) Prespawning behavior, spawning, and development of the brooding starfish Leptasterias polaris. Biol Bull 188:32–45CrossRefGoogle Scholar
  9. Harrold C, Pearse JS (1980) Allocation of pyloric caecum reserves in fed and starved sea stars, Pisaster giganteus (Stimpson): somatic maintenance comes before reproduction. J Exp Mar Biol Ecol 48:169–183CrossRefGoogle Scholar
  10. Hendler G (1991) Echinodermata: Ophiuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, vol 6. The Boxwood Press, Pacific Grove, pp 356–511Google Scholar
  11. Himmelman JH, Dumont CP, Gaymer CF, Vallières C, Drolet D (2008) Spawning synchrony and aggregative behavior of cold-water echinoderms during multi-species mass spawnings. Mar Ecol Prog Ser 361:161–168CrossRefGoogle Scholar
  12. Jangoux M (1982) Food and feeding mechanisms: Asteroidea. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. AA Balkema, Rotterdam, pp 117–159Google Scholar
  13. Keesing JK, Heine JN, Babcock RC, Craig PD and Koslow JA (2006) Strategic research fund for the marine environment final report. The SRFME core projects, Vol 2. Strategic research fund for the marine environment, CSIRO, Australia, p 266Google Scholar
  14. Kendrick GA, Langtry S, Fitzpatrick J, Griffiths R, Jacoby CA (1998) Benthic microalgae and nutrient dynamics in wave-disturbed environments in Marmion lagoon, Western Australia, compared with less disturbed mesocosms. J Exp Mar Biol Ecol 228:83–105CrossRefGoogle Scholar
  15. Komatsu M (1983) Development of the sea-star, Archaster typicus, with a note on male-on-female superposition. Annot Zool Jpn 56:187–195Google Scholar
  16. Lawrence JM, Lane JM (1982) The utilisation of resources by post-metamorphic echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. A.A. Balkema, Rotterdam, pp 331–371Google Scholar
  17. Lawrence JM, Klinger TS, McClintock JB, Watts SA, Chen C-P, Marsh A, Smith L (1986) Allocation of nutrient resources to body components by regenerating Luidia clathrata (Say) Echinodermata : Asteroidea). J Exp Mar Biol Ecol 102:47–53Google Scholar
  18. Lawrence JM, Keesing JK, Irvine TR (2010) Observations on aggregated pseudo-copulation of the sea star Archaster angulatus Müller & Troschel, 1842 (Echinodermata: Asteroidea) in south-western Australia. J Mar Biol Assoc UK doi: 10.1017/S0025315410000871
  19. Levitan DR (1998) Sperm limitation, sperm competition and sexual selection in external fertilizers. In: Birkhead T, Møller A (eds) Sperm competition and sexual selection. Academic Press, San Diego, pp 173–215Google Scholar
  20. Lourey MJ, Dunn JR, Waring J (2006) A mixed-layer nutrient climatology of Leeuwin Current and Western Australian shelf waters: seasonal nutrient dynamics and biomass. J Mar Syst 59(1–2):25–51CrossRefGoogle Scholar
  21. McEuen FS (1988) Spawning behaviors of northeast Pacific sea cucumbers (Holothuroidea: Echinodermata). Mar Biol 98:565–585CrossRefGoogle Scholar
  22. Mortensen T (1931) Contributions to the study of the development and larval forms of echinoderms I & II. Konngelige Danske Videnskabeernes Sekskabs Naturvidenskabelige og Mathematiske Afhandlingner 4:1–39Google Scholar
  23. Morton B (1976) Selective site segregation in Balcis shaplandi and Mucronalia fulvescens (Mollusca: Gastropoda: Aglossa) parasitic upon Archaster typicus (Echinodermata: Asteroidea). Malacol Rev 9:55–61Google Scholar
  24. Morton B (1979) The population dynamics and expression of sexuality in Balcis shaplandi and Mucronalia fulvescens (Mollusca: Gastropoda: Aglossa) parasitic upon Archaster typicus (Echinodermata: Asteroidea). Malacologia 18:327–346Google Scholar
  25. Mukai H, Nishihara M, Kamisato H, Fujimoto Y (1986) Distribution and abundance of the sea-star Archaster typicus in Kabira Cove, Ishigaki Island, Okinawa. Bull Mar Sci 38:366–383Google Scholar
  26. Nojima S (1983) Ecological studies of the sea star, Astropecten latespinosus Meissner. V. Pattern of spatial distribution and seasonal migration, with special reference to spawning aggregation. Publ Amakusa Mar Biol Lab 7(1):1–16Google Scholar
  27. Ohshima H, Ikeda H (1934a) Sexual size-dimorphism in the sea star Archaster typicus. Müll. et Trosch. Proc Imperial Acad Jpn 10:180–183Google Scholar
  28. Ohshima H, Ikeda H (1934b) Male-female superposition of the sea-star Archaster typicus Müll. et Trosch. Proc Jpnese Acad Tokyo 10:125–128Google Scholar
  29. Parrish CC, Deibel D, Thompson RJ (2009) Effect of sinking spring phytoplankton blooms on lipid content and composition in suprabenthic and benthic invertebrates in a cold ocean coastal environment. Mar Ecol Prog Ser 391:33–51CrossRefGoogle Scholar
  30. Pearce A, Rossbach M, Tait M, Brown R (1999) Sea temperature variability off Western Australia 1990 to 1994. Fish Res Rep Fish West Aust 111:1–45Google Scholar
  31. Run J-Q, Chen C-P, Chang K-Y, Chia F-S (1988) Mating behaviour and reproductive cycle of Archaster typicus (Echinodermata: Asteroidea). Mar Biol 99:247–253CrossRefGoogle Scholar
  32. Shick JM, Taylor WF, Lamb AN (1981a) Reproduction and genetic variation in the deposit-feeding sea star Ctenodiscus crispatus. Mar Biol 63:51–66CrossRefGoogle Scholar
  33. Shick JM, Edwards KC, Dearborn JH (1981b) Physiological ecology of the deposit-feeding sea star Ctenodiscus crispatus: ciliated surfaces and animal-sediment interactions. Mar Ecol Prog Ser 5:165–184CrossRefGoogle Scholar
  34. Slattery M, Bosch I (1993) Mating behaviour of a brooding Antarctic asteroid, Neosmilaster georgianus. Invert Reprod Devel 24:97–102CrossRefGoogle Scholar
  35. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. W.H, Freeman, p 859Google Scholar
  36. Tominaga H, Komatsu M, Oguro C (1994) Aggregation and spawning in the breeding season of the sea-star, Asterina minor Hayashi. In: David B, Guille A, Feral J-P, Roux M (eds) Echinoderms through time: proceedings of the 8th international echinoderm conference, Dijon, France, 6–10 September 1993. AA Balkema, Rotterdam, pp 369–373Google Scholar
  37. Tominaga H, Nakamura S, Komatsu M (2004) Reproduction and development of the conspicuously dimorphic brittle star Ophiodaphne formata (Ophiuroidea). Biol Bull 206:25–34CrossRefGoogle Scholar
  38. Tyler PA, Young CM, Billett DSM, Giles LA (1992) Pairing behaviour, reproduction and diet in the deep-sea holothurian genus Paroriza (Holothurioidea: Synallactidae). J Mar Biol Ass UK 72:447–462CrossRefGoogle Scholar
  39. Unger B, Lott C (1994) In situ studies on the aggregation behaviour of the sea urchin Sphaerechinis granularis Lam. (Echinodermata: Echinoidea). In: David B, Guille A, Feral J-P, Roux M (eds) Echinoderms through time: proceedings of the 8th international echinoderm conference, Dijon, France, 6–10 September 1993. AA Balkema, Rotterdam, pp 913–919Google Scholar
  40. Young CM, Tyler PA, Cameron JL, Rumrill SG (1992) Seasonal breeding aggregations in low-density populations of the bathyal echinoid Stylocidaris lineata. Mar Biol 113:603–612CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • John K. Keesing
    • 1
  • Fiona Graham
    • 1
  • Tennille R. Irvine
    • 1
  • Ryan Crossing
    • 1
  1. 1.CSIRO Wealth from Oceans Flagship, Marine and Atmospheric ResearchWembleyAustralia

Personalised recommendations