Marine Biology

, Volume 156, Issue 8, pp 1659–1671 | Cite as

Gametogenic and reproductive cycles of the sea anemone, Entacmaea quadricolor

  • Anna ScottEmail author
  • Peter Lynton Harrison
Original Paper


Host sea anemones are ecologically important as they provide habitat for obligate symbiotic anemonefish in many areas of the Indo-Pacific. Despite their importance, no information is available on their gametogenic cycles. This study aimed to address this lack of knowledge by determining the gametogenic cycles of Entacmaea quadricolor. Gonad samples were taken from January 2003 to February 2005 at North Solitary Island, Solitary Islands Marine Park, Australia using a specially developed non-lethal field biopsy sampling technique. Sampling was done 17 times during the study period, with 15–20 individuals being sampled on each occasion. Samples were examined prior to fixation, and then histologically sectioned to determine the reproductive activity of each individual. Female anemones were significantly more abundant than males, and had asynchronous oocyte development both within and among individuals. Male anemones showed a single annual cycle of spermary growth, development and spawning. Data from the 26-month study indicated that spawning occurred in the austral summer and autumn between January and April, which coincided with the observed spawning periods that have previously been documented for this species in outdoor flow-through seawater tanks at the study location. The biopsy sampling technique used during this study provides an opportunity to gain a more thorough understanding of the gametogenic cycles and sexual pattern of host sea anemones throughout their distribution.


Germinal Vesicle Colour Morph Oocyte Development Gametogenic Cycle Gastrovascular Cavity 
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.



Special thanks to T. Baillie and T. Jones from the Coffs Harbour Base Hospital Pathology Unit who contributed a significant amount of time and expertise during the preparation of the histological sections for this study. We are grateful to everyone who volunteered their time during field work, especially C. Damiano, A. Carroll, J. Rowland and R. Forbes. This paper forms part of a PhD dissertation submitted by A. Scott to Southern Cross University, Lismore. This research was supported by grants from the Australian Geographic Society, Project AWARE Asia Pacific, NSW Marine Parks Authority and SCU Postgraduate grants. Research was conducted in accordance with the conditions specified by NSW Fisheries Permit P02/0025 and complied with the current laws of Australia.


  1. Babcock RC, Mundy CN, Keesing J, Oliver J (1992) Predictable and unpredictable spawning events: in situ behavioural data from free-spawning coral reef invertebrates. Invertebr Reprod Dev 22:213–228CrossRefGoogle Scholar
  2. Braley RD (1984) Reproduction in the giant clams Tridacna gigas and T. derasa in situ on the north-central Great Barrier Reef, Australia, and Papua New Guinea. Coral Reefs 4:221–227. doi: CrossRefGoogle Scholar
  3. Bronsdon SK, Tyler PA, Gage JD, Rice AL (1993) Reproductive biology of two epizoic anemones from the deep north-eastern Atlantic Ocean. J Mar Biol Assoc UK 73:531–542CrossRefGoogle Scholar
  4. Bucklin A (1982) The annual cycle of sexual reproduction in the sea anemone Metridium senile. Can J Zool 60:3241–3248. doi: CrossRefGoogle Scholar
  5. Bucklin A (1985) Biochemical genetic variation, growth and regeneration of the sea anemone Metridium of British shores. J Mar Biol Assoc UK 65:141–157CrossRefGoogle Scholar
  6. Carter MA, Funnell ME (1980) Reproduction and brooding in Actinia. In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Elsevier, Amsterdam, pp 17–22Google Scholar
  7. Carter MA, Miles J (1989) Gametogenic cycles and reproduction in the beadlet sea anemone Actinia equina (Cnidaria: Anthozoa). Biol J Linn Soc Lond 36:129–155. doi: CrossRefGoogle Scholar
  8. Chia F, Rostron MA (1970) Some aspects of the reproductive biology of Actinia equina (Cnidaria: Anthozoa). J Mar Biol Assoc UK 50:253–264CrossRefGoogle Scholar
  9. Chia F, Lutzen J, Svane I (1989) Sexual reproduction and larval morphology of the primitive anthozoan Gonactinia prolifera M. Sars J Exp Mar Biol Ecol 127:13–24. doi: CrossRefGoogle Scholar
  10. Clark WHJ, Dewel WC (1974) The structure of the gonads, gametogenesis, and sperm-egg interactions in the Anthozoa. Am Zool 14:495–510CrossRefGoogle Scholar
  11. Dunn DF (1975) Reproduction of the externally brooding sea anemone Epiactis prolifera Verrill, 1869. Biol Bull 148:199–218. doi: CrossRefGoogle Scholar
  12. Dunn DF (1977) Dynamics of external brooding in the sea anemone Epiactis prolifera. Mar Biol (Berl) 39:41–49. doi: CrossRefGoogle Scholar
  13. Dunn DF (1981) The clownfish sea anemones: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Trans Am Philos Soc 71:1–115. doi: CrossRefGoogle Scholar
  14. Dunn DF (1982) Sexual reproduction of two intertidal sea anemones (Coelenterata: Actiniaria) in Malaysia. Biotropica 14:262–271. doi: CrossRefGoogle Scholar
  15. Dunn DF (1983) Some antarctic and sub-antarctic sea anemones (Coelenterata: Ptychodactiaria and Actiniara). Ant Res 39:1–67Google Scholar
  16. Fautin DG, Allen GR (1997) Anemone fishes and their host sea anemones: a guide for aquarists and divers. Western Australian Museum, PerthGoogle Scholar
  17. Ford CEJ (1964) Reproduction in the aggregating sea anemone, Anthopleura elegantissima. Pac Sci 18:138–145Google Scholar
  18. Francis L (1973) Clone specific segregation in the sea anemone Anthopleura elegantissima. Biol Bull 144:64–72. doi: CrossRefGoogle Scholar
  19. Fukui Y (1995) Seasonal changes in testicular structure of the sea anemone Haliplanella lineata (Coelenterata, Actiniaria). Invertebr Reprod Dev 27:197–204CrossRefGoogle Scholar
  20. Glynn PW, Colley SB, Ting JH, Mate JL, Guzman HM (2000) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama and Galapagos Islands (Ecuador). IV. Agariciidae, recruitment and recovery of Pavona varians and Pavona sp.a. Mar Biol (Berl) 136:785–805. doi: CrossRefGoogle Scholar
  21. Goffredo S, Arnone S, Zaccanti F (2002) Sexual reproduction in the Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Mar Ecol Prog Ser 229:83–94. doi: CrossRefGoogle Scholar
  22. Goffredo S, Radetic J, Airi V, Zaccanti F (2005) Sexual reproduction of the solitary sunset cup coral Leptopsammia pruvoti (Scleractinia: Dendrophylliidae) in the Mediterranean. 1. Morphological aspects of gametogenesis and ontogenesis. Mar Biol (Berl) 147(48):5–495. doi: Google Scholar
  23. Gomes PB, Zamponi MO, Sole-Cava AM (2003) Asexual reproduction and molecular systematics of the sea anemone Anthopleura krebsi (Actiniaria: Actiniidae). Rev Biol Trop 51:147–154PubMedGoogle Scholar
  24. Harrison PL, Jamieson BGM (1999) Cnidaria and Ctenophora. In: Jamieson BGM (ed) Reproductive biology of the invertebrates, Vol IX Part A, progress in male gamete ultrastructure and phylogeny. Oxford-IBH, New Delhi, pp 21–95Google Scholar
  25. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs. Elsevier, Amsterdam, pp 133–207Google Scholar
  26. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189. doi: CrossRefGoogle Scholar
  27. Hirose Y (1985) Habitat, distribution and abundance of coral reef sea-anemones (Actiniidea and Stichodactylidae) in Sesoko Island, Okinawa, with notes on expansion and contraction behavior. Galaxea 4:113–127Google Scholar
  28. Jennison BL (1978) Effects of thermal effluents on reproduction in the sea anemone. In: Thorp JH, Gibbons JW (eds) Energy and environmental stress in aquatic systems. DOE Symposium Series (CONF-771114). National Technical Information Service, Springfield, pp 470–483Google Scholar
  29. Jennison BL (1979) Gametogenesis and reproductive cycles in the sea anemone Anthopleura elegantissima (Brandt, 1935). Can J Zool 57:403–411. doi: CrossRefGoogle Scholar
  30. Jennison BL (1981) Reproduction in three species of sea anemones from Key West, Florida. Can J Zool 59:1708–1719CrossRefGoogle Scholar
  31. Larkman A (1980) Ultrastructural aspects of gametogenesis in Actinia equina L. In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Amsterdam, Elsevier, pp 61–66Google Scholar
  32. Larkman AU (1981) An ultrastructural investigation of the early stages of oocyte differentiation in Actinia fragacea (Cnidaria; Anthozoa). Int J Invertebr Reprod 4:147–167CrossRefGoogle Scholar
  33. Larkman AU, Carter MA (1982) Preliminary ultrastructural and autoradiographic evidence that the trophonema of the sea anemone Actinia fragacea has a nutritive function. Int J Invertebr Reprod 4:375–379CrossRefGoogle Scholar
  34. Levitan DR (1991) Influence of body size and population density on fertilisation success and reproductive output in a free-spawning invertebrate. Biol Bull 181:261–268. doi: CrossRefGoogle Scholar
  35. Lin MD, Chen CLA, Fang LS (2001) Distribution and sexual reproduction of a seagrass-bed-inhabiting actiniarian, Phymanthus strandesi (Cnidaria: Anthozoa: Actiniaria: Phymanthidae), at Hsiao-Licuchiu, Taiwan. Zool Stud 40:254–261Google Scholar
  36. Maynard-Smith J (1978) The evolution of sex. Cambridge University Press, CambridgeGoogle Scholar
  37. MPA (2002) Overview of the zoning plan: Solitary Islands Marine Park. Marine Parks Authority, Coffs HarbourGoogle Scholar
  38. Neves EG, Pires DO (2002) Sexual reproduction of Brazilian coral Mussismilia hispida (Verrill, 1902). Coral Reefs 21:161–168Google Scholar
  39. Olive PJW (1995) Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J Therm Biol 20:79–90. doi: CrossRefGoogle Scholar
  40. Oliver J, Babcock R (1992) Aspects of the fertilisation ecology of broadcast spawning corals: sperm dilution effects and in situ measurements of fertilisation. Biol Bull 183:409–417. doi: CrossRefGoogle Scholar
  41. Ottaway JR (1979) Population ecology of the intertidal anemone Actinia tenebrosa II. Geographical distribution, synonymy, reproductive cycle and fecundity. Aust J Zool 27:273–290. doi: CrossRefGoogle Scholar
  42. Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival. Hydrobiologia 530–531:513–520. doi: Google Scholar
  43. Schmidt H, Höltken B (1980) Peculiarities of spermatogenesis and sperm in Anthozoa. In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Elsevier, Amsterdam, pp 53–59Google Scholar
  44. Scott A, Harrison PL (2005) Synchronous spawning of host sea anemones. Coral Reefs 24:208. doi: CrossRefGoogle Scholar
  45. Scott A, Harrison PL (2007) Broadcast spawning of two species of sea anemone, Entacmaea quadricolor and Heteractis crispa, that host anemonefish. Invertebr Reprod Dev 50:163–171CrossRefGoogle Scholar
  46. Sebens KP (1981) Reproductive ecology of the intertidal sea anemones Anthopleura xanthogrammica and A. elegantissima: body size, habitat, and sexual reproduction. J Exp Mar Biol Ecol 54:225–250. doi: CrossRefGoogle Scholar
  47. Shaw PW (1989) Seasonal patterns and possible long-term effectiveness of sexual reproduction in three species of sagartiid sea anemones. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distributions of marine organisms. lsen and Olsen, Denmark, pp 189–199Google Scholar
  48. Shick JM (1991) A functional biology of sea anemones. Chapman and Hall, LondonCrossRefGoogle Scholar
  49. Shuman CS, Hodgson G, Ambrose RF (2005) Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines. Coral Reefs 24:564–573. doi: CrossRefGoogle Scholar
  50. Spaulding JG (1974) Embryonic and larval development in sea anemones (Anthozoa: Actiniaria). Am Zool 14:511–520CrossRefGoogle Scholar
  51. Szmant A (1991) Sexual reproduction by the Caribbean reef corals Montastrea annularis and M. cavernosa. Mar Ecol Prog Ser 74:13–25. doi: CrossRefGoogle Scholar
  52. Van-Praët M (1990) Gametogenesis and the reproductive cycle in the deep-sea anemone Paracalliactis stephensoni (Cnidaria: Actiniaria). J Mar Biol Assoc UK 70:163–172CrossRefGoogle Scholar
  53. Van-Praët M, Rice AL, Thurston MH (1990) Reproduction in two deep-sea anemones (Actiniaria); Phelliactis hertwigi and P. robusta. Prog Oceanogr 24:207–222. doi: CrossRefGoogle Scholar
  54. Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar Biol (Berl) 88:217–233. doi: CrossRefGoogle Scholar
  55. Wedi SE, Dunn DF (1983) Gametogenesis and reproductive periodicity of the subtidal sea anemone Urticina lofotensis (Coelenterata: Actiniaria) in California. Biol Bull 165:458–472. doi: CrossRefGoogle Scholar
  56. Willis BL, Babcock RC, Harrison PL, Oliver JK (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. In: Proceedings of 5th International Coral Reef Congress 4:343–348Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.National Marine Science CentreCoffs Harbour JettyAustralia
  2. 2.Coral Reef Research Centre, School of Environmental Science and ManagementSouthern Cross UniversityLismoreAustralia

Personalised recommendations