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Broadcast Spawning by Pocillopora Species on the Great Barrier Reef

  • Sebastian Schmidt-Roach ,

    s.schmidt-roach@aims.gov.au

    Affiliations Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Australia, Australian Institute of Marine Science, Townsville, Queensland, Australia

  • Karen J. Miller,

    Affiliation Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Australia

  • Erika Woolsey,

    Affiliation Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia

  • Gabriele Gerlach,

    Affiliation Carl von Ossietzky University Oldenburg, Institute for Biology and Environmental Sciences, Oldenburg, Germany

  • Andrew H. Baird

    Affiliation Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia

Broadcast Spawning by Pocillopora Species on the Great Barrier Reef

  • Sebastian Schmidt-Roach, 
  • Karen J. Miller, 
  • Erika Woolsey, 
  • Gabriele Gerlach, 
  • Andrew H. Baird
PLOS
x

Abstract

The coral genus Pocillopora is one of the few to include some species that broadcast spawn gametes and some species that brood larvae, although reports of reproductive mode and timing vary within and among species across their range. Notably, the ubiquitous Pocillopora damicornis has been described as both a brooder and spawner, although evidence of broadcast spawning is rare. Here, we report observations of broadcast-spawning in four species of Pocillopora on the Great Barrier Reef (GBR), including P. damicornis. All species spawned predictably during the early morning, two days following the full moon, and spawning was observed in multiple months over the summer period (November to February). Eggs and sperm were free-spawned concurrently. Eggs were negatively buoyant and contained Symbiodinium. This newfound knowledge on the mode, timing and regularity of broadcast spawning in Pocillopora spp. on the GBR brings us one step closer to elucidating the complex reproductive ecology of these species.

Introduction

Much conjecture exists about the reproductive biology of the coral genus Pocillopora despite it representing one of the most abundant and widely studied taxa of scleractinian corals. The genus is one of the few to include species that brood larvae (e.g. P. damicornis) and species that broadcast spawn gametes (e.g. P. eydouxi; [1][2]). Spawning in corals refers to the release of gametes into the water column for external fertilisation and larval development, whereas brooding refers to the development of planula larvae within the polyps [3]. Brooded planulae may originate from internal fertilization of eggs or from parthenogenesis [2]. The ecological and evolutionary consequences of such a diversity of reproductive modes within a single coral genus has been the subject of considerable research over the last decades (e.g. [4][5], [6][7]), although there still remain many gaps in our knowledge about when, and how, most Pocillopora spp. reproduce.

Pocillopora damicornis is thought to brood throughout most of its range (Table 1), and in Western Australia, Eastern Australia and Taiwan, molecular analysis indicate that brooded larvae are produced largely asexually [4][6], [7][8]. Other earlier examples of Pocillopora spp. brooding larvae have been discredited [3], except for one recent observation in the Philippines (P. verrucosa; [9]). In summary, of the seventeen formally accepted species of Pocillopora [10], three (P. eydouxi, P. meandrina, P. elegans) are broadcast spawners and two (P. verrucosa and P. damicornis) have a different mode of larval development among regions. In addition, some P. damicornis reproduce by brooding larvae and spawning gametes (Table 1).

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Table 1. Reproductive mode of Pocillopora species (*inferred from histology).

https://doi.org/10.1371/journal.pone.0050847.t001

At least some of the controversy around spatial variation in the reproductive mode of Pocillopora spp. is likely to be linked to the existence of cryptic species. For example, P. damicornis is now recognised to be a species complex rather than a single morphologically plastic species [11]. Of the five putative species within the P. damicornis complex, three were observed brooding (and at least two brood asexual larvae; Table 1). Spawning has been reported for P. cf. damicornis in the Eastern-Pacific [12], although evidence shows that this species actually resolves genetically within one clade with P. verrucosa and P. damicornis Type γ and thus is genetically distant to species observed brooding in Australia [11]. Clearly, the difficulties in distinguishing even among what are considered morphologically distinct species of Pocillopora has contributed to the conflicting reports on reproductive behaviour within species.

The mode of reproduction in P. damicornis is also a matter of conjecture. Like many species, spawning has never been observed in P. damicornis rather, it has been inferred from the disappearance of gametes in histological samples [5][12], [13]. In Australia, as in most other areas, all planula larvae examined appear to have been produced asexually [4][6], [7][11], however, the population genetic structure reflects random sexual reproduction with high genotypic diversity (e.g. [7][14]) suggesting important aspects of the life history of P. damicornis remain unknown. Here, we report the first observation of broadcast spawning of gametes in four Pocillopora species, including P. damicornis, and suggest that sexual reproduction is likely to occur regularly in pocilloporids on the GBR.

Materials and Methods

All necessary permits were obtained for the described field studies. The samples were taken under Permit No G10/33440.1 issued to the Australian Institute for Marine Science by the Great Barrier Reef Marine Park Authority (GRBMPA) and Permit No 2011/158501 issued to Sebastian Schmidt-Roach by the Rottnest Island Authority.

Colonies of four Pocillopora species were collected 1–2 days before the full moon and maintained in a flow through seawater aquarium system at One Tree Island Research Station (23°30′29S; 152°4′37E) (P. damicornis) and Lizard Island Research Station (P. eydouxi, P. verrucosa and P. meandrina) (14°41′58S; 145°26′54E) in the summer of 2011/2012. The flow-through water was turned off around midnight every night for up to 20 days following full moon to enable spawning to be observed. In addition to specimens observed to spawn (a total of ten colonies; Table 2), at Lizard Island two colonies of P. damicornis Type α (sensu Schmidt-Roach et al [11]) and two specimens of P. verrucosa were isolated, but did not spawn. Specimens were visually identified and categorised according to Veron [10] and Schmidt-Roach et al. [11]. For a subset of specimens belonging to each morphotype, identification was further verified by sequencing of the mitochondrial ORF region [15] following protocols described in Schmidt-Roach et al. [11]. Furthermore, differences in the population ecology of P. damicornis from Western Australia (population structure predominantly asexual; [16][17]) and P. damicornis in Eastern Australia (population structure predominantly sexual; [18][19], [6][14], [7]) suggest these might be different species. Consequently, six specimens of P. damicornis from Rottnest Island, WA, were genotyped and sequences compared to existing data from the GBR. The alignment consisted of 11 sequences and 590 bp (NCBI accession numbers: JX983175-JX983186); reference sequences of previously identified cryptic species [11] were additionally included in the analysis to identify and illustrate the genealogical relationships amongst the taxa investigated in this study (NCBI accession numbers: JX985589; JX985612; JX985610; JX985592; JX985613; JX985605). Phylogenetic hypotheses were generated in MEGA4 [20] using the Neighbor-Joining algorithm under the JC correction and 100.000 bootstrap pseudo-replicated for nodal support [21][22].

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Figure 2. Spawning Pocillopora meandrina at Trimodal Reef, Lizard Island.

https://doi.org/10.1371/journal.pone.0050847.g002

Results and Discussion

During the southern hemisphere summer of 2011/12 we observed gamete release in Pocillopora eydouxi, P. verrucosa and P. meandrina at Lizard Island, and P. damicornis at One Tree Island (Table 2); two locations at opposite ends of the GBR. Genotyping of 590 bp of the mitochondrial ORF region confirmed identifications based on morphology, except for P. meandrina and P. eydouxi, which share the same mitochondrial lineage [23], and therefore can not be distinguished by this marker. Spawning in all species occurred 1–2 days following the full moon, approximately 45 min after sunrise and continued for 2–3 hrs. Unlike most broadcast spawning coral species, Pocillopora gametes were free-spawned separately, rather than packaged in egg-sperm bundles. Sperm release was evident as a dense cloud surrounding the colony (Fig. 1 & 2). Due to the small size (see below), eggs were difficult to see, explaining why this behaviour may have been missed previously (e.g. [5][24]). The eggs were negatively buoyant, approximately 80 µm in diameter, and could easily be collected by siphoning the bottom of the aquaria below the colony. Eggs of P. meandrina (Fig. 3; Movie S1) and P. eydouxi contained algal symbionts, Symbiodinium. Ethanol preserved sperm samples of P. damicornis from One Tree Island also contained eggs. These eggs were 50–60 µm, which matches the size of mature P. damicornis eggs in histological sections [5][13] (Fig. S1). This strongly suggests the spawned eggs were mature rather than immature oocytes released due to handling. Fertilisation trials are required to confirm this unequivocally. Nevertheless, the release of sperm and mature eggs concurrently strongly suggests that sexual reproduction will occur. Numerous studies on sexual reproduction in other scleractinian corals (e.g. [25][26], [27]) have demonstrated that spawning behaviour in the laboratory is identical to that in the wild. Thus broadcast spawning of gametes with external fertilisation and larval development is likely to be the spawning behaviour in the field and the source of the sexual recruits of P. damicornis reported by previous studies (e.g. [6]).

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Figure 3. Brooded planula (Pocillopora damicornis, left) next to a spawned egg (Pocillopora meandrina, top right), indicating the size difference in Pocillopora between brooded and spawned offspring.

https://doi.org/10.1371/journal.pone.0050847.g003

Our observations are in agreement with reports from Hawaii [28][29], [30], Japan [31] and the Red Sea [32] regarding time and mode of larval development in these Pocillopora species, suggesting daytime spawning with a lunar periodicity may be characteristic for this genus across its range. Importantly, for P. damicornis this is the first direct observation of gamete release. In addition, brooded planulae were released the night before gamete release, indicating that both reproductive strategies occur simultaneously in the same colony supporting the inferences of previous histological studies [5][13]. Other coral species are known to vary their mode of reproduction in different geographic regions; however, Goniastrea aspera is the only other species in which individual colonies both brood and spawn [33].

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Figure 4. Mitochondrial phylogeny of Pocillopora specimens based on the ORF region.

Coloured bars denote genetically distinct lineages or cryptic species identified by Schmidt-Roach et al [11]. Pocillopora eydouxi and Pocillopora meandrina shared identical mitochondrial haplotypes whilst Pocillopora verrucosa was recovered within the same clade with P. damicornis Type γ. Pocillopora damicornis Type σ and Type β were added in the phylogeny to indicate the close genetic relationship of brooding species within the genus Pocillopora. Black and white vertical bars indicate the proposed reproductive strategies of these taxa in Australia. Sample locations, indicated by three letter codes, are as follows: OTI = One Tree Island; ROT = Rottnest Island; LZI = Lizard Island. Numbers represent bootstrap values.

https://doi.org/10.1371/journal.pone.0050847.g004

Histological studies have suggested that P. damicornis in Western Australia both spawns and broods (at Rottnest Island: [5]) and that the brooded larvae are generated asexually [4]. Sequence data confirmed that Western Australian specimens are genetically identical to P. damicornis Type α [11] on the east coast of Australia (Fig. 4). Our observations on the GBR of spawning in a lineage of P. damicornis known to brood, the release of brooded larvae and spawning over consecutive nights in the same colony, as well as the overwhelming evidence that brooded planulae are generated asexually [6], [7], [11] suggests the same is true of P. damicornis on the east coast of Australia. Consequently brooding lineages within P. damicornis throughout Australia most likely have a mixed mode of reproduction (Fig. 4). Indeed, the clonal generation of planulae seems to be characteristic of these lineages within Pocillopora [11] (Fig. 4), which contrasts with the sexual brooding reported in the sister genera Stylophora and Seriatopora [34][35], [36].

The evolutionary advantages of a mixed mode of asexual brooding and sexual spawning are still poorly understood. While settlement behavior and competency periods of brooded larvae of P. damicornis lineages are well studied (e.g. [37][38], [39]), nothing is known of the larval biology of spawned larvae in Pocillopora. Therefore, our observations represent an important foundation for future studies to further elucidate the differences between these larval types and the selective advantages of each mode of reproduction.

Typically for species with mixed modes of reproduction, asexual reproduction contributes to maintenance of local populations, with sexual progeny used for dispersal and recruitment to distant areas (i.e. the strawberry-coral model of Williams [40]). However, population genetic studies of P. damicornis on the GBR [18][19], [6][7] show only limited evidence of local recruitment of asexual planulae, but genetic subdivision even on relatively small spatial scales among populations suggests dispersal of sexual larvae is also limited. Thus there is little evidence that P. damicornis conforms to the predictions of the strawberry-coral model. It may be that the opposite occurs within P. damicornis, with the sexual progeny from broadcast spawning settling locally (as occurs for other broadcast spawning species – [19][41], [42][43]) and the larger, and potentially better-provisioned asexual larvae being more widely dispersed. Indeed, Richmond [37] reported that some brooded larvae of P. damicornis remained competent for over 100 days suggesting widespread dispersal of brooded larvae is possible. To date, population genetic studies have shown only limited evidence that asexual larvae of P. damicornis could be more widely dispersed, for example Ayre & Miller [6] found colonies with identical genotypes on opposite sides of One Tree Reef. If these corals represent recruitment from asexual planulae, then dispersal on the scale of kilometers may well occur.

Clearly further research is required to tease apart the roles of the two larval types in P. damicornis and their dispersal potential. Striking differences in size of the asexual (∼1000 µm) and sexual (∼80 µm) (Fig. 3) larvae suggest dispersal potential may well vary between them, although both types do contain zooxanthellae and therefore have the potential to be autotrophic [1]. Furthermore, the size difference raises questions of skeletal differences in early settlement between brooded and spawned larvae. While the skeletons of recruits of brooded offspring in this family are well studied [44] and often a focus of recruitment studies (e.g. [45]), the small size of spawned larvae may result in observable differences in size between sexual and asexual recruits and thus may enable the brooded and spawned recruits to be distinguished at settlement, similar to recruits in Porites spp. [46]. The predictable and consecutive spawning over several months that we report here makes Pocillopora ideal for future experiments to address such questions, as well as aspects of both the ecological and evolutionary processes in this important group of corals, including the maintenance of mixed mode of reproduction and hybridization in the genus Pocillopora [47–23], [11].

Supporting Information

Figure S1.

Sperm and eggs of Pocillopora damicornis (after fixation in ethanol).

https://doi.org/10.1371/journal.pone.0050847.s001

(EPS)

Movie S1.

Spawning Pocillopora meandrina at Trimodal Reef, Lizard Island.

https://doi.org/10.1371/journal.pone.0050847.s002

(M4V)

Acknowledgments

The authors would like to thank the staff of One Tree Island and Lizard Island research station for their field support and A. Schmidt-Roach for comments on the manuscript. Tania Mendo for field assistance at Rottnest Island. N. Andreakis for advice and suggestions.

Author Contributions

Conceived and designed the experiments: SS-R KM. Analyzed the data: SS-R. Contributed reagents/materials/analysis tools: SS-R KM AB. Prepared and executed the field experiments with helpful assistance from the remaining authors: SS-R. Prepared the manuscript with helpful assistance from the remaining authors: SS-R.

References

  1. 1. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annual Review of Ecology, Evolution and Systematics 40: 551–571.
  2. 2. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N, editors. Coral Reefs: An Ecosystem in Transition Part 3. Springer Dordrecht Heidelberg, London, New York, 59–85.
  3. 3. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z, editor. Coral Reefs. Elsevier, Amsterdam, 133–207.
  4. 4. Stoddart J (1983) Asexual production of planulae in the coral Pocillopora damicornis. Mar Biol 76: 279–284.
  5. 5. Ward S (1992) Evidence for broadcast spawning as well as brooding in the scleractinian coral Pocillopora damicornis. Mar Biol 112: 641–646.
  6. 6. Ayre DJ, Miller KJ (2004) Where do clonal coral larvae go? Adult genotypic diversity conflicts with reproductive effort in the brooding coral Pocillopora damicornis. Mar Ecol Prog Ser 277: 95–105.
  7. 7. Sherman CDH, Ayre DJ, Miller KJ (2006) Asexual reproduction does not produce clonal populations of the brooding coral Pocillopora damicornis on the Great Barrier Reef, Australia. Coral Reefs 25: 7–18.
  8. 8. Yeoh SR, Dai CF (2010) The production of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis. Mar Biol 157: 351–359.
  9. 9. Villanueva R, Yap H, Montaño M (2008) Timing of planulation by pocilloporid corals in the northwestern Philippines. Mar Ecol Prog Ser 370: 111–119.
  10. 10. Veron JEN (2000) Corals of the world, Volume 2. Townsville, Australia: Australian Institute of Marine Science. 429.
  11. 11. Schmidt-Roach S, Lundgren P, Miller KJ, Gerlach G, Noreen AME, et al.. (2012) Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs. DOI: 10.1007/s00338-012-0959-z.
  12. 12. Glynn PW, Gassman NJ, Eakin CM, Cortés J, Smith DB, et al. (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá, and Galápagos Islands (Ecuador). Mar Biol 109: 355–368.
  13. 13. Muir P (1984) Periodicity and asexual planulae production in Pocillopora damicornis (Linnaeus) at Magnetic Island. Honours Thesis, James Cook University, p60.
  14. 14. Miller KJ, Ayre DJ (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92: 557–568.
  15. 15. Flot J-F, Tillier S (2007) The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: The putative D-loop and a novel ORF of unknown function. Gene 401: 80–87.
  16. 16. Stoddart J (1984) Genetic differentiation amongst populations of the coral Pocillopora damicornis off southwestern Australia. Coral Reefs 3: 149–156.
  17. 17. Stoddart J (1984) Genetical structure within populations of the coral Pocillopora damicornis. Mar Biol 81: 19–30.
  18. 18. Benzie JAH, Haskell A, Lehman H (1995) Variation in the genetic composition of coral (Pocillopora damicornis and Acropora palifera) populations from different reef habitats. Mar Biol 121: 731–739.
  19. 19. Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54: 1590–1605.
  20. 20. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol24: 1596–1599.
  21. 21. Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.
  22. 22. Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
  23. 23. Flot J-F, Magalon H, Cruaud C, Couloux A, Tillier S (2008) Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. Comptes Rendus Biologies 331: 239–247.
  24. 24. Séré MG, Massé LM, Perissinotto R, Schleyer MH (2010) Influence of heterotrophic feeding on the sexual reproduction of Pocillopora verrucosa in aquaria. J Exp Mar Biol Ecol 395: 63–71.
  25. 25. Miller KJ, Babcock R (1997) Conflicting morphological and reproductive species boundaries in the coral genus Platygyra. Biol Bull 192: 98–110.
  26. 26. Willis B, Babcock R, Harrison P, Wallace C (1997) Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16: 53–65.
  27. 27. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, et al. (1986) Synchronous spawning of 105 scleractinian coral species on the Great Barrier Reef. Marine Biology 90: 379–394.
  28. 28. Fiene-Severns P (1998) A note on synchronous spawning in the reef coral Pocillopora meandrina at Molokini Islet, Hawaii. Reproduction in Reef Corals. E. F. Cox, University of Hawaii. Technical Report No.42.
  29. 29. Riddle D (2008) Coral reproduction, part one: A natural coral spawning in Hawaii, The cauliflower coral (Pocillopora meandrina). Advanced Aquarist's Online Magazine 7: 10–16.
  30. 30. Riddle D, Peck S (2009) A first report: Pocillopora eydouxi spawning in Hawaii, and other observations. Available: http://www.coralscience.org/main/articles/reproduction-10/pocillopora-eydouxi. Accessed 25 July 2012.
  31. 31. Kinzie III R (1993) Spawning in the reef corals Pocillopora verrucosa and P. eydouxi at Sesoko Island, Okinawa. Galaxea 11: 93–105.
  32. 32. Bouwmeester J, Berumen M, Baird AH (2011) Daytime broadcast spawning of Pocillopora verrucosa on coral reefs of the central Red Sea. Galaxea 13: 23–24.
  33. 33. Sakai K (1997) Gametogenesis, spawning, and planula brooding by the reef coral Goniastrea aspera (Scleractinia) in Okinawa, Japan. Mar Ecol Prog Ser 151: 67–72.
  34. 34. Ayre DJ, Resing JM (1986) Sexual and asexual production of planulae in reef corals. Mar Biol 90: 187–190.
  35. 35. Sherman CDH (2007) Mating system variation in the hermaphroditic brooding coral, Seriatopora hystrix. Heredity 100: 296–303.
  36. 36. Douek J, Amar K-O, Rinkevich B (2011) Maternal-larval population genetic traits in Stylophora pistillata, a hermaphroditic brooding coral species. Genetica 139: 1531–1542.
  37. 37. Richmond RH (1987) Energetic, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93: 527–533.
  38. 38. Harii S, Kayanne H, Takigawa H, Hayashibara T, Yamamoto M (2002) Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Mar Biol 141: 39–46.
  39. 39. Cumbo VR, Fan T-Y, Edmunds PJ (2012) Physiological development of brooded larvae from two pocilloporid corals in Taiwan. Mar Biol DOI:10.1007/s00227-012-2046-y.
  40. 40. Williams GC (1975) Sex and evolution. Monogr Popul Biol 8: 3–200.
  41. 41. Miller KJ, Ayre D (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. J Anim Ecol. 77: 713–724.
  42. 42. Combosch DJ, Vollmer SV (2011) Population Genetics of an Ecosystem-Defining Reef Coral Pocillopora damicornis in the Tropical Eastern Pacific. PLoS ONE 6: e21200 DOI:10.1371/journal.pone.0021200.
  43. 43. Paz-García DA, Chávez-Romo HE, Correa-Sandoval F, Reyes-Bonilla H, López-Pérez A, et al. (2012) Genetic Connectivity Patterns of Corals Pocillopora damicornis and Porites panamensis (Anthozoa: Scleractinia) Along the West Coast of Mexico. Pac Sci 66: 43–61.
  44. 44. Baird AH, Babcock RC (2000) Morphological differences among three species of newly settled pocilloporid coral recruits. Coral Reefs 19: 179–183.
  45. 45. Schmidt-Roach S, Kunzmann A, Arbizu PM (2008) In situ observation of coral recruitment using fluorescence census techniques. J Exp Mar Biol Ecol 367: 37–40.
  46. 46. Babcock RC, Baird AH, Piromvaragorn S, Thomson DP, Willis BL (2003) Identification of scleractinian coral recruits from Indo-Pacific reefs. Zool Stud 42: 211–226.
  47. 47. Combosch DJ, Guzman HM, Schuhmacher H, Vollmer SV (2008) Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Mol Ecol 17: 1304–1312.
  48. 48. Fadlallah Y (1985) Reproduction in the coral Pocillopora verrucosa on the reefs adjacent to the industrial city of Yanbu (Red Sea, Saudi Arabia). Proc 5th Int Coral Reef Cong 4: 313–318.
  49. 49. Shlesinger Y, Loya Y (1985) Coral community reproductive patterns: Red Sea versus the Great Barrier Reef. Science 228: 1333–1335.
  50. 50. Sier C, Olive P (1994) Reproduction and reproductive variability in the coral Pocillopora verrucosa from the Republic of Maldives. Mar Biol 118: 713–722.
  51. 51. Hirose M, Kinzie R, Hidaka M (2000) Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae. Biol Bull 199: 68–75.
  52. 52. Stimson J (1978) Mode and timing of reproduction in some common hermatypic corals of Hawaii and Enewetak. Mar Biol 48: 173–184.
  53. 53. Stoddart JA, Black R (1985) Cycles of gametogenesis and planulation in the coral Pocillopora damicornis. Mar Ecol Prog Ser 23: 153–164.
  54. 54. Rodríguez-Troncoso AP, Carpizo-Ituarte E, Leyte-Morales GE, Chi-Barragán G, Tapia-Vázquez O (2011) Sexual reproduction of three coral species from the Mexican South Pacific. Mar Biol DOI: 10.1007/s00227-011-1765-9.
  55. 55. Marshall SM, Stephenson TA (1933) The breeding of reef animals. Part I. The corals. Sci Rep Great Barrier Reef Exped 1928-29 3: 219–245.
  56. 56. Harriott V (1983) Reproductive ecology of four scleratinian species at Lizard Island, Great Barrier Reef. Coral Reefs 2: 9–18.
  57. 57. Tanner JE (1996) Seasonality and lunar periodicity in the reproduction of pocilloporid corals. Coral Reefs 15: 59–66.
  58. 58. Kuanui P, Chavanich S, Raksasab C, Viyakarn V (2008) Lunar periodicity of larval release and larval development of Pocillopora damicornis in Thailand. Mar Freshw Res 11: 375–377.
  59. 59. Richmond RH, Jokiel PL (1984) Lunar Periodicity in Larva Release in the Reef Coral Pocillopora damicornis at Enewetak and Hawaii. Bull Mar Sci 34: 280–287.