Behavioral Ecology and Sociobiology

, Volume 64, Issue 11, pp 1749–1765

Synchronized breeding events in sympatric marine invertebrates: role of behavior and fine temporal windows in maintaining reproductive isolation

Original Paper


While breeding synchrony among conspecifics is increasingly well understood with regards to the reproductive success of vertebrate and invertebrate taxa, the occurrence of simultaneous multispecies breeding events remains intriguing. The fairly recent discovery of mass annual spawnings in reef corals has provided a first glimpse at putative strategies of reproductive isolation during such events. However, the mechanisms and advantages of same-day heterospecific breeding are still poorly understood and have not yet been investigated in non-coral taxa with different life history strategies. In an effort to bridge this gap, we investigated spawning periodicity and synchrony among 26 sympatric species of free-spawning, capsule-laying, and brood-protecting macroinvertebrates belonging to six different phyla. Twenty-four of these species released gametes or larvae between early March and late April. We analyzed the events over fine temporal scales to test the hypothesis that breeding activities were not random in time or relative to each other. We found that the two main reproductive pulses followed a lunar periodicity and that consistent species- and gender-specific modulations in the timing of spawning occurred during same-day episodes involving up to six free-spawning species. Mass spawning accounts from the literature were reviewed and compared. This work suggests that many species participate in synchronous heterospecific spawning events either because they respond to the same environmental cues or rely on cross-cueing and that reproductive isolation is favored by species-specific circadian patterns, spawning behaviors and cross-gender signaling.


Breeding synchrony Spawning behavior Marine invertebrate Species interaction Lunar periodicity Reproduction 

Supplementary material

265_2010_987_MOESM1_ESM.pdf (52 kb)
Fig. S1Breeding periodicities recorded in free-spawning species in 2007 (open bars show males; solid bars show females). The moon phases are shown (open circle full moon; filled circle new moon), with grayed areas identifying the period between the first and last moon quarters. Scale of x-axis matches that of Fig. 1 for easier comparison (PDF 52 kb)
265_2010_987_MOESM2_ESM.pdf (36 kb)
Fig. S2Circular histograms of spawnings recorded in March and April 2007 for six free-spawning species (Fig. S1). Data shown as frequency of occurrence on each lunar day. Filled circle new moon; open circle full moon (PDF 35 kb)


  1. Andries J-C (2001) Endocrine and environmental control of reproduction in Polychaeta. Can J Zool 79:254–270CrossRefGoogle Scholar
  2. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394CrossRefGoogle Scholar
  3. Babcock R, Mundy C, Keesing J, Oliver J (1992) Predictable and unpredictable spawning events: in situ behavioural data from free-spawning coral reef invertebrates. Invertebr Reprod Dev 22:213–227Google Scholar
  4. Brady A, Hilton J, Vize P (2009) Coral spawn timing is a direct response to solar light cycles and is not an entrained circadian response. Coral Reefs 28:677–680CrossRefGoogle Scholar
  5. Carroll A, Harrison P, Adjeroud M (2006) Sexual reproduction of Acropora reef corals at Moorea, French Polynesia. Coral Reefs 25:93–97CrossRefGoogle Scholar
  6. De Bruyn AMH, Meeuwig JJ (2001) Detecting lunar cycles in marine ecology: periodic regression versus categorical ANOVA. Mar Ecol Prog Ser 214:307–310CrossRefGoogle Scholar
  7. Fukami H, Omori M, Shimoike K, Hayashibara T, Hatta M (2003) Ecological and genetic aspects of reproductive isolation by different spawning times in Acropora corals. Mar Biol 142:679–684Google Scholar
  8. Gaudette J, Wahle RA, Himmelman JH (2006) Spawning events in small and large populations of the green sea urchin Strongylocentrotus droebachiensis as recorded using fertilization assays. Limnol Oceanogr 51:1485–1496CrossRefGoogle Scholar
  9. Gemmill JF (1914) The development and certain points in the adult structure of the starfish Asterias rubens, L. Philos Trans R Soc Lond B Biol Sci 205:213–294CrossRefGoogle Scholar
  10. Giese AC (1959) Comparative physiology: annual reproductive cycles of marine invertebrates. Annu Rev Physiol 21:547–576CrossRefPubMedGoogle Scholar
  11. Giese AC, Pearse JS, Pearse VB (1991) Reproduction of marine invertebrates. In, vol 6, echinoderms and lophophorates. Boxwood, Pacific GroveGoogle Scholar
  12. Gotceitas V, Methven DA, Fraser S, Brown JA (1999) Effects of body size and food ration on over-winter survival and growth of age-0 Atlantic cod, Gadus morhua. Environ Biol Fish 54:413–420CrossRefGoogle Scholar
  13. Guest JR (2008) From molecules to moonbeams: spawning synchrony in coral reef organisms. Invertebr Reprod Dev 51:145–149Google Scholar
  14. Guest JR, Baird AH, Goh BPL, Chou LM (2005) Seasonal reproduction in equatorial reef corals. Invertebr Reprod Dev 48:207Google Scholar
  15. Hagman DK, Vize PD (2003) Mass spawning by two brittle star species, Ophioderma rubicundum and O. squamosissimum (Echinodermata: Ophiuroidea), at the Flower Garden Banks, Gulf of Mexico. Bull Mar Sci 72:871–876Google Scholar
  16. Hamel J-F, Mercier A (1994) Occurrence of interspecific cross-fertilization among echinoderms and mollusks. Invertebr Reprod Dev 26:221–228Google Scholar
  17. Hamel J-F, Mercier A (1995) Spawning of the sea cucumber Cucumaria frondosa in the St Lawrence Estuary, eastern Canada. SPC Beche-de-mer Inf Bull 7:12–18Google Scholar
  18. Hamel J-F, Mercier A (1996) Evidence of chemical communication during the gametogenesis of holothuroids. Ecology 77:1600–1616CrossRefGoogle Scholar
  19. Hamel J-F, Mercier A (1999) Mucus as a mediator of gametogenic synchrony in the sea cucumber Cucumaria frondosa (Holothuroidea: Echinodermata). J Mar Biol Assoc UK 79:121–129CrossRefGoogle Scholar
  20. Hamel J-F, Sargent P, Mercier A (2008) Diet, reproduction, settlement and growth of Palio dubia (Nudibranchia: Polyceridae) in the north-west Atlantic. J Mar Biol Assoc UK 88:365–374CrossRefGoogle Scholar
  21. Harper FM, Hart MW (2005) Gamete compatibility and sperm competition affect paternity and hybridization between sympatric Asterias sea stars. Biol Bull 209:113–126CrossRefPubMedGoogle Scholar
  22. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinski Z (ed) Ecosystems of the world, vol 25, Coral reefs. Elsevier Science, Amsterdam, pp 133–207Google Scholar
  23. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189CrossRefPubMedGoogle Scholar
  24. Hart MW, Scheibling RE (1988) Heat waves, baby booms, and the destruction of kelp beds by sea urchins. Mar Biol 99:167–176CrossRefGoogle Scholar
  25. Hendler G (1991) Echinodermata: Ophiuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates Vol. 6. The Boxwood, Pacific Grove, pp 355–511Google Scholar
  26. Himmelman JH (1999) Spawning, marine invertebrates. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic, New York, pp 524–533Google Scholar
  27. Himmelman JH, Dumont CP, Gaymer CF, Vallières C, Drolet D (2008) Spawning synchrony and aggregative behaviour of cold-water echinoderms during multi-species mass spawnings. Mar Ecol Prog Ser 361:161–168CrossRefGoogle Scholar
  28. Ims RA (1990) On the adaptive value of reproductive synchrony as a predator-swamping strategy. Am Nat 136:485–498CrossRefGoogle Scholar
  29. Kubota H (1981) Synchronization of spawning in the crinoid, Comanthus japonica. In: Clark WH Jr, Adams TS (eds) Advances in invertebrate reproduction. Elsevier/North Holland, New York, pp 69–74Google Scholar
  30. Levitan DR (2005) Sex-specific spawning behavior and its consequences in an external fertilizer. Am Nat 165:682–694CrossRefPubMedGoogle Scholar
  31. Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308–323PubMedGoogle Scholar
  32. Marsden JR (1987) Coral preference behaviour by planktotrophic larvae of Spirobranchus giganteus corniculatus (Serpulidae: Polychaeta). Coral Reefs 6:71–74CrossRefGoogle Scholar
  33. McClary DJ, Mladenov PV (1989) Reproductive pattern in the brooding and broadcasting sea star Pteraster militaris. Mar Biol 103:531–540CrossRefGoogle Scholar
  34. McEuen FS (1986) The reproductive biology and development of twelve species of holothuroids from the San Juan Islands, Washington. PhD thesis, University of AlbertaGoogle Scholar
  35. McEuen FS (1988) Spawning behaviors of northeast Pacific sea cucumbers (Holothuroidea: Echinodermata). Mar Biol 98:565–585CrossRefGoogle Scholar
  36. McGuire MP (1998) Timing of larval release by Porites astreoides in the northern Florida Keys. Coral Reefs 17:369–375CrossRefGoogle Scholar
  37. Mercier A, Hamel J-F (2008) Depth-related shift in life history strategies of a brooding and broadcasting deep-sea asteroid. Mar Biol 156:205–223Google Scholar
  38. Mercier A, Hamel J-F (2009) Endogenous and exogenous control of gametogenesis and spawning in echinoderms. Adv Mar Biol 55:1–302CrossRefGoogle Scholar
  39. Mercier A, Ycaza RH, Hamel J-F (2007) Long-term study of gamete release in a broadcast-spawning holothurian: predictable lunar and diel periodicities. Mar Ecol Prog Ser 329:179–189CrossRefGoogle Scholar
  40. Minchin D (1992) Multiple species, mass spawning events in an Irish sea lough: the effect of temperatures on spawning and recruitment of invertebrates. Invertebr Reprod Dev 22:229–238Google Scholar
  41. Naylor E (1999) Marine animal behaviour in relation to lunar phase. Earth Moon Planet 85–86:291–302CrossRefGoogle Scholar
  42. Olive PJW (1995) Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J Therm Biol 20:79–90CrossRefGoogle Scholar
  43. Omori K (1995) The adaptive significance of a lunar or semi-lunar reproductive cycle in marine animals. Ecol Model 82:41–49CrossRefGoogle Scholar
  44. Pearse JS, McClary DJ, Sewell MA, Austin WC, Perez-Ruzafa A, Byrne M (1988) Simultaneous spawning of six species of echinoderms in Barkley Sound, British Columbia, Canada. Int J Inver Rep Dev 14:279–288Google Scholar
  45. Penland L, Kloulechad J, Idip D, Woesik R (2004) Coral spawning in the western Pacific Ocean is related to solar insolation: evidence of multiple spawning events in Palau. Coral Reefs 23:133–140CrossRefGoogle Scholar
  46. Petrie B, Akenhead SA, Lazier SA, Loder J (1988) The cold intermediate layer on the Labrador and Northeast Newfoundland Shelves, 1978–86. NAFO Sci Counc Stud 12:57–69Google Scholar
  47. Reitzel AM, Miner BG, McEdward LR (2004) Relationships between spawning date and larval development time for benthic marine invertebrates: a modeling approach. Mar Ecol Prog Ser 280:13–23CrossRefGoogle Scholar
  48. Scheibling RE, Metaxas A (2008) Abundance, spatial distribution, and size structure of the sea star Protoreaster nodosus in Palau, with notes on feeding and reproduction. Bull Mar Sci 82:221–235Google Scholar
  49. Sewell MA, Levitan DR (1992) Fertilization success during a natural spawning of the dendrochirote sea cucumber Cucumaria miniata. Bull Mar Sci 51:161–166Google Scholar
  50. So J (2009) Assessment of the biology, ecology and gene flow of the sea cucumber Cucumaria frondosa for management of the fishery in the Newfoundland and Labrador region. MSc Thesis, Memorial UniversityGoogle Scholar
  51. Starr M, Himmelman JH, Therriault J-C (1990) Direct coupling of marine invertebrate spawning with phytoplankton blooms. Science 247:1071–1074CrossRefPubMedGoogle Scholar
  52. Strathmann RR (1979) Echinoid larvae from the northeast Pacific (with a key and comment on an unusual type of planktotrophic development). Can J Zool 57:610–616CrossRefGoogle Scholar
  53. Strathmann MF (1987) Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press, SeattleGoogle Scholar
  54. Van Veghel MLJ (1993) Multiple species spawning on Curaçao reefs. Bull Mar Sci 52:1017–1021Google Scholar
  55. Vize PD, Embesi JA, Nickell M, Brown DP, Hagman DK (2005) Tight temporal consistency of coral mass spawning at the Flower Garden Banks, Gulf of Mexico, from 1997–2003. Gulf Mex Sci 23:107–114Google Scholar
  56. Wasson KM, Watts SA (2007) Endocrine regulation of sea urchin reproduction. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 55–69Google Scholar
  57. Watson GJ, Bentley MG, Gaudron SM, Hardege JD (2003) The role of chemical signals in the spawning induction of polychaete worms and other marine invertebrates. J Exp Mar Biol Ecol 294:169–187CrossRefGoogle Scholar
  58. Yamaguchi M (1973) Early life histories of coral reef asteroids with special reference to Acanthaster planci. In: Jones OA, RE (eds) Biology and geology of coral reefs, Vol. 2. Academic Press New York, New York, pp 369–387Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Ocean Sciences Centre (OSC)Memorial UniversitySt. John’sCanada
  2. 2.Society for the Exploration and Valuing of the Environment (SEVE)St. PhilipsCanada

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