Advertisement

Sexual Reproduction of Scleractinian Corals in Mesophotic Coral Ecosystems vs. Shallow Reefs

  • Tom ShlesingerEmail author
  • Yossi Loya
Chapter
Part of the Coral Reefs of the World book series (CORW, volume 12)

Abstract

Corals utilize sex-derived diversity to adapt to environmental changes and to occupy new ecological niches. With major declines in coral reefs worldwide and calls for ecosystem-based management, understanding how environmental gradients affect coral reproductive performance over a species’ range and within a demographically relevant timescale is critical. The study of coral reproduction is a mature field with the reproductive aspects of more than 450 species recorded. However, the vast majority of coral reproduction studies have been on shallow reefs, while knowledge of reproduction in mesophotic coral ecosystems (MCEs) is sparse. This knowledge gap hinders our ability to assess the resilience and functionality of MCEs and to understand ecosystem-scale connectivity. Environmental factors that influence coral reproduction, such as light, temperature, and disturbances, can vary dramatically with depth. Sexual reproduction has evolved, partly, to address environmental pressures. We, therefore, expect that environmental parameters can influence reproductive patterns and success. There is currently insufficient information to allow conclusions to be drawn regarding the effects of mesophotic depths on the phenology of coral reproduction, other than it might differ from shallow reefs. Nonetheless, it appears that reproductive performance decreases with depth, with most of the species studied so far in MCEs having exhibited either reduced fecundity or reduced oocyte size compared to shallower populations. Here, we summarize the current knowledge on mesophotic coral reproduction and propose several hypotheses regarding the changes in coral reproductive traits across depth and their implications for population connectivity and persistence. Additionally, we highlight crucial knowledge gaps and recommend future research.

Keywords

Coral reproduction Mesophotic coral ecosystems Fecundity Reproductive phenology Reproductive success 

Notes

Acknowledgments

We thank the Interuniversity Institute for Marine Sciences (IUI) in Eilat and YL’s lab members for their support. We are grateful to N. Paz for editing the manuscript. We would like to thank the three peer reviewers including Selina Ward, Joana Figueiredo, and an anonymous reviewer. This research was funded by the Israel Science Foundation (ISF) Grants No. 341/12 and 1191/16 to YL and the Israel Taxonomy Initiative and Rieger Foundation Fellowship to TS.

References

  1. Akkaynak D, Treibitz T, Shlesinger T, Tamir R, Loya Y, Iluz D (2017) What is the space of attenuation coefficients in underwater computer vision. In: Proceedings of the IEEE Computer Vision and Pattern Recognition Conference (CVPR), Honolulu, Hawaii, 21–26 July 2017Google Scholar
  2. Appeldoorn R, Ballantine D, Bejarano I, Carlo M, Nemeth M, Otero E, Pagan F, Ruiz H, Schizas N, Sherman C, Weil E (2016) Mesophotic coral ecosystems under anthropogenic stress: a case study at Ponce, Puerto Rico. Coral Reefs 35:63–75CrossRefGoogle Scholar
  3. Atoda K (1947) The larva and postlarval development of some reef-building corals. Pocillopora damicornis cespitosa (DANA). Sci Rep Tohoku Univ 4th Ser (Biol) 18:24–47Google Scholar
  4. Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605PubMedGoogle Scholar
  5. 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 90:379–394Google Scholar
  6. Baird AH, Babcock RC, Mundy CP (2003) Habitat selection by larvae influences the depth distribution of six common coral species. Mar Ecol Prog Ser 252:289–293Google Scholar
  7. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571Google Scholar
  8. Birkeland C, Green A, Fenner D, Squair C, Dahl AL (2013) Substratum stability and coral reef resilience: insights from 90 years of disturbances on a reef in American Samoa. Micronesica 6:1–16Google Scholar
  9. Bongaerts P, Smith TB (2019) Beyond the “Deep Reef Refuge” hypothesis: a conceptual framework to characterize persistence at depth. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 881–895Google Scholar
  10. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘Deep Reef Refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327CrossRefGoogle Scholar
  11. Bongaerts P, Frade PR, Ogier JJ, Hay KB, van Bleijswijk J, Englebert N, Vermeij MJ, Bak RP, Visser PM, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2-60 m) on a Caribbean reef. BMC Evol Biol 13:205PubMedPubMedCentralGoogle Scholar
  12. Bongaerts P, Riginos C, Brunner R, Englebert N, Smith SR, Hoegh-Guldberg O (2017) Deep reefs are not universal refuges: reseeding potential varies among coral species. Sci Adv 3:e1602373PubMedPubMedCentralGoogle Scholar
  13. Bridge TCL, Hughes TP, Guinotte JM, Bongaerts P (2013a) Call to protect all coral reefs. Nat Clim Chang 3:528–530Google Scholar
  14. Bridge TCL, Hoey AS, Campbell SJ, Muttaqin E, Rudi E, Fadli N, Baird AH (2013b) Depth-dependent mortality of reef corals following a severe bleaching event: implications for thermal refuges and population recovery. F1000Res 2:187PubMedGoogle Scholar
  15. Charnov EL (1982) The theory of sex allocation. Princeton University Press, PrincetonGoogle Scholar
  16. Connolly SR, Baird AH (2010) Estimating dispersal potential for marine larvae: dynamic models applied to scleractinian corals. Ecology 91:3572–3583PubMedGoogle Scholar
  17. Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kühl M, Muirhead A, O’Leary RA, Ziersen BE, van Oppen MJH (2011) Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc R Soc B 278:1840–1850PubMedGoogle Scholar
  18. Crandall JB, Teece MA, Estes BA, Manfrino C, Ciesla JH (2016) Nutrient acquisition strategies in mesophotic hard corals using compound specific stable isotope analysis of sterols. J Exp Mar Biol Ecol 474:133–141Google Scholar
  19. Cunning R, Gillette P, Capo T, Galvez K, Baker AC (2015) Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34:155–160Google Scholar
  20. Einbinder S, Mass T, Brokovich E, Dubinsky Z, Erez J, Tchernov D (2009) Changes in morphology and diet of the coral Stylophora pistillata along a depth gradient. Mar Ecol Prog Ser 381:167–174Google Scholar
  21. Emlet RB, Hoegh-Guldberg O (1997) Effects of egg size on postlarval performance: experimental evidence from a sea urchin. Evolution 51:141–152PubMedGoogle Scholar
  22. Eyal-Shaham L, Eyal G, Tamir R, Loya Y (2016) Reproduction, abundance and survivorship of two Alveopora spp. in the mesophotic reefs of Eilat, Red Sea. Sci Rep 6:20964PubMedPubMedCentralGoogle Scholar
  23. Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Mol Ecol 18:2375–2389PubMedGoogle Scholar
  24. Feldman B, Shlesinger T, Loya Y (2018) Mesophotic coral-reef environments depress the reproduction of the coral Paramontastraea peresi in the Red Sea. Coral Reefs 37:201–214Google Scholar
  25. Figueiredo J, Baird AH, Connolly SR (2013) Synthesizing larval competence dynamics and reef-scale retention reveals a high potential for self-recruitment in corals. Ecology 94:650–659PubMedGoogle Scholar
  26. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71Google Scholar
  27. Gilmour JP, Underwood JN, Howells EJ, Gates E, Heyward AJ (2016) Biannual spawning and temporal reproductive isolation in Acropora corals. PLoS ONE 11:e0150916PubMedPubMedCentralGoogle Scholar
  28. Gorbunov MY, Falkowski PG (2002) Photoreceptors in the cnidarian hosts allow symbiotic corals to sense blue moonlight. Limnol Oceanogr 47:309–315Google Scholar
  29. Gorospe KD, Karl SA (2013) Genetic relatedness does not retain spatial pattern across multiple spatial scales: dispersal and colonization in the coral, Pocillopora damicornis. Mol Ecol 22:3721–3736PubMedGoogle Scholar
  30. Goulet TL, Lucas MQ, Schizas NV (2019) Symbiodiniaceae genetic diversity and symbioses with hosts from shallow to mesophotic coral ecosystems. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 537–551Google Scholar
  31. Graham EM, Baird AH, Connolly SR (2008) Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27:529–539Google Scholar
  32. Graham NA, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97PubMedGoogle Scholar
  33. Harii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Mar Biol 157:1215–1224Google Scholar
  34. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinski Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 59–85Google Scholar
  35. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinski Z (ed) Ecosystems of the world. Elsevier, Amsterdam, pp 133–207Google Scholar
  36. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189PubMedGoogle Scholar
  37. Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep 5:12407PubMedPubMedCentralGoogle Scholar
  38. Holstein DM, Smith TB, Paris CB (2016a) Depth-independent reproduction in the reef coral Porites astreoides from shallow to mesophotic zones. PLoS ONE 11:e0146068PubMedPubMedCentralGoogle Scholar
  39. Holstein DM, Paris CB, Vaz AC, Smith TB (2016b) Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35:23–37Google Scholar
  40. Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2000) Supply-side ecology works both ways: the link between benthic adults, fecundity, and larval recruits. Ecology 81:2241–2249Google Scholar
  41. Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JB, Kleypas J, van de Leemput IA, Lough JM, Morrison TH, van Nes EH, Scheffer M (2017) Coral reefs in the Anthropocene. Nature 546:82–90PubMedGoogle Scholar
  42. Isomura N, Nishihira M (2001) Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals. Coral Reefs 20:309–315Google Scholar
  43. Jerlov NG (1976) Marine optics. Elsevier, New YorkGoogle Scholar
  44. Jones AM, Berkelmans R (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium type-D. J Mar Biol 2011:185890Google Scholar
  45. Kahng SE, Copus JM, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81Google Scholar
  46. Kahng SE, Akkaynak D, Shlesinger T, Hochberg EJ, Wiedenmann J, Tamir R, Tchernov D (2019) Light, temperature, photosynthesis, heterotrophy, and the lower depth limits of mesophotic coral ecosystems. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 801–828Google Scholar
  47. Keith SA, Maynard JA, Edwards AJ, Guest JR, Bauman AG, van Hooidonk R, Heron SF, Berumen ML, Bouwmeester J, Piromvaragorn S, Rahbek C, Baird AH (2016) Coral mass spawning predicted by rapid seasonal rise in ocean temperature. Proc R Soc B 283:20160011PubMedGoogle Scholar
  48. Keshavmurthy S, Hsu C-M, Kuo C-Y, Denis V, Leung JK-L, Fontana S, Hsieh HJ, Tsai W-L, Su W-C, Chen CA (2012) Larval development of fertilized “pseudo-gynodioecious” eggs suggests a sexual pattern of gynodioecy in Galaxea fascicularis (Scleractinia: Euphyllidae). Zool Stud 51:143–149Google Scholar
  49. Kramarsky-Winter E, Loya Y (1998) Reproductive strategies of two fungiid corals from the northern Red Sea: environmental constraints? Mar Ecol Prog Ser 174:175–182Google Scholar
  50. Lesser MP, Slattery M (2011) Phase shift to algal dominated communities at mesophotic depths associated with lionfish (Pterois volitans) invasion on a Bahamian coral reef. Biol Invasions 13:1855–1868Google Scholar
  51. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8Google Scholar
  52. Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli A (2010) Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics. Ecology 91:990–1003Google Scholar
  53. Leuzinger S, Willis BL, Anthony KR (2012) Energy allocation in a reef coral under varying resource availability. Mar Biol 159:177–186Google Scholar
  54. Levitan DR (1996) Effects of gamete traits on fertilization in the sea and the evolution of sexual dimorphism. Nature 382:153Google Scholar
  55. Levitan DR, Fogarty ND, Jara J, Lotterhos KE, Knowlton N (2011) Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex. Evolution 65:1254–1270PubMedGoogle Scholar
  56. Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, Hoegh-Guldberg O (2007) Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318:467–470PubMedGoogle Scholar
  57. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494PubMedGoogle Scholar
  58. Loya Y (1976) The Red Sea coral Stylophora Pistillata is an r strategist. Nature 259:478–480Google Scholar
  59. Loya Y, Sakai K (2008) Bidirectional sex change in mushroom stony corals. Proc R Soc B 275:2335–2343PubMedGoogle Scholar
  60. Loya Y, Eyal G, Treibitz T, Lesser MP, Appeldoorn R (2016) Theme section on mesophotic coral ecosystems: advances in knowledge and future perspectives. Coral Reefs 35:1–9Google Scholar
  61. Marshall DJ, Keough MJ (2007) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60PubMedGoogle Scholar
  62. Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype–environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140PubMedGoogle Scholar
  63. Mendes J, Woodley J (2002) Timing of reproduction in Montastraea annularis: relationship to environmental variables. Mar Ecol Prog Ser 227:241–251Google Scholar
  64. Miller SW, Hayward DC, Bunch TA, Miller DJ, Ball EE, Bardwell VJ, Zarkower D, Brower DL (2003) A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evol Dev 5:251–258PubMedGoogle Scholar
  65. Muir PR, Marshall PA, Abdulla A, Aguirre JD (2017) Species identity and depth predict bleaching severity in reef-building corals: shall the deep inherit the reef? Proc R Soc B 284:20171551PubMedGoogle Scholar
  66. Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563PubMedGoogle Scholar
  67. Mundy C, Babcock R (1998) Role of light intensity and spectral quality in coral settlement: implications for depth-dependent settlement? J Exp Mar Biol Ecol 223:235–255Google Scholar
  68. Mundy C, Babcock R (2000) Are vertical distribution patterns of scleractinian corals maintained by pre-or post-settlement processes? A case study of three contrasting species. Mar Ecol Prog Ser 198:109–119Google Scholar
  69. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinski Z (ed) Ecosystems of the world. Elsevier, New York, pp 75–87Google Scholar
  70. Nitschke MR, Davy SK, Ward S (2016) Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment. Coral Reefs 35:335–344Google Scholar
  71. Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719PubMedGoogle Scholar
  72. Padilla-Gamiño JL, Pochon X, Bird C, Concepcion GT, Gates RD (2012) From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS ONE 7:e38440PubMedPubMedCentralGoogle Scholar
  73. Pochon X, Forsman ZH, Spalding HL, Padilla-Gamiño JL, Smith CM, Gates RD (2015) Depth specialization in mesophotic corals (Leptoseris spp.) and associated algal symbionts in Hawaiʻi. R Soc Open Sci 2:140351PubMedPubMedCentralGoogle Scholar
  74. Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Natl Acad Sci U S A 110:3961–3966PubMedPubMedCentralGoogle Scholar
  75. Prasetia R, Sinniger F, Harii S (2016) Gametogenesis and fecundity of Acropora tenella (Brook 1892) in a mesophotic coral ecosystem in Okinawa, Japan. Coral Reefs 35:53–62Google Scholar
  76. Prasetia R, Sinniger F, Hashizume K, Harii S (2017a) Reproductive biology of the deep brooding coral Seriatopora hystrix: implications for shallow reef recovery. PLoS ONE 12:e0177034PubMedPubMedCentralGoogle Scholar
  77. Prasetia R, Sinniger F, Harii S (2017b) First record of spawning in the mesophotic Acropora tenella in Okinawa, Japan. Galaxea J Coral Reef Stud 19:5–6Google Scholar
  78. Rapuano H, Brickner I, Shlesinger T, Meroz-Fine E, Tamir R, Loya Y (2017) Reproductive strategies of the coral Turbinaria reniformis in the northern Gulf of Aqaba (Red Sea). Sci Rep 7:42670PubMedPubMedCentralGoogle Scholar
  79. Richmond RH (1987a) Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533Google Scholar
  80. Richmond RH (1987b) Energetic relationships and biogeographical differences among fecundity, growth and reproduction in the reef coral Pocillopora damicornis. Bull Mar Sci 41:594–604Google Scholar
  81. Richmond RH (1997) Reproduction and recruitment in corals: critical links in the persistence of reefs. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, New York, pp 175–197Google Scholar
  82. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals – comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203Google Scholar
  83. Rinkevich B, Loya Y (1987) Variability in the pattern of sexual reproduction of the coral Stylophora pistillata at Eilat, Red Sea: a long-term study. Biol Bull 173:335–344Google Scholar
  84. Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij MJ, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci 38:437–457Google Scholar
  85. Rosser NL, Thomas L, Stankowski S, Richards ZT, Kennington WJ, Johnson MS (2017) Phylogenomics provides new insight into evolutionary relationships and genealogical discordance in the reef-building coral genus Acropora. Proc R Soc B 284:20162182PubMedGoogle Scholar
  86. Semmler RF, Hoot WC, Reaka ML (2017) Are mesophotic coral ecosystems distinct communities and can they serve as refugia for shallow reefs? Coral Reefs 36:433–444Google Scholar
  87. Serrano XM, Baums IB, O’Reilly K, Smith TB, Jones RJ, Shearer TL, Nunes FLD, Baker AC (2014) Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Mol Ecol 23:4226–4240PubMedPubMedCentralGoogle Scholar
  88. Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC (2016) Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep 6:21619PubMedPubMedCentralGoogle Scholar
  89. Shlesinger T, Loya Y (2016) Recruitment, mortality, and resilience potential of scleractinian corals at Eilat, Red Sea. Coral Reefs 35:1357–1368Google Scholar
  90. Shlesinger T, Grinblat M, Rapuano H, Amit T, Loya Y (2018) Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt. Ecology 99:421–437PubMedPubMedCentralGoogle Scholar
  91. Shlesinger Y, Loya Y (1985) Coral community reproductive patterns – Red Sea versus the Great Barrier Reef. Science 228:1333–1335PubMedGoogle Scholar
  92. Shlesinger Y, Goulet TL, Loya Y (1998) Reproductive patterns of scleractinian corals in the northern Red Sea. Mar Biol 132:691–701Google Scholar
  93. Smith TB, Gyory J, Brandt ME, Miller WJ, Jossart J, Nemeth RS (2016) Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Glob Chang Biol 22:2756–2765Google Scholar
  94. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  95. Strader ME, Davies SW, Matz MV (2015) Differential responses of coral larvae to the colour of ambient light guide them to suitable settlement microhabitat. R Soc Open Sci 2:150358PubMedPubMedCentralGoogle Scholar
  96. Sweeney AM, Boch CA, Johnsen S, Morse DE (2011) Twilight spectral dynamics and the coral reef invertebrate spawning response. J Exp Biol 214:770–777PubMedGoogle Scholar
  97. Thomas CJ, Bridge TCL, Figueiredo J, Deleersnijder E, Hanert E (2015) Connectivity between submerged and near-sea-surface coral reefs: can submerged reef populations act as refuges? Divers Distrib 21(10):1254–1266Google Scholar
  98. Thomson DP, Bearham D, Graham F, Eagle JV (2011) High latitude, deeper water coral bleaching at Rottnest Island, Western Australia. Coral Reefs 30:1107Google Scholar
  99. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784PubMedGoogle Scholar
  100. van Woesik R (2009) Calm before the spawn: global coral spawning patterns are explained by regional wind fields. Proc R Soc B 277:715–722PubMedGoogle Scholar
  101. van Woesik R, Lacharmoise F, Köksal S (2006) Annual cycles of solar insolation predict spawning times of Caribbean corals. Ecol Lett 9:390–398PubMedGoogle Scholar
  102. Vaz AC, Paris CB, Olascoaga MJ, Kourafalou VH, Kang H, Reed JK (2016) The perfect storm: match-mismatch of bio-physical events drives larval reef fish connectivity between Pulley Ridge mesophotic reef and the Florida Keys. Cont Shelf Res 125:136–146Google Scholar
  103. Vize PD (2006) Deepwater broadcast spawning by Montastraea cavernosa, Montastraea franksi, and Diploria strigosa at the Flower Garden Banks, Gulf of Mexico. Coral Reefs 25:169–171Google Scholar
  104. Vollmer SV, Palumbi SR (2006) Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs. J Hered 98:40–50PubMedGoogle Scholar
  105. Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar Biol 88:217–233Google Scholar
  106. Warner PA, Willis BL, van Oppen MJH (2016) Sperm dispersal distances estimated by parentage analysis in a brooding scleractinian coral. Mol Ecol 25:1398–1415PubMedGoogle Scholar
  107. Wellington GM, Fitt WK (2003) Influence of UV radiation on the survival of larvae from broadcast-spawning reef corals. Mar Biol 143:1185–1192Google Scholar
  108. West S (2009) Sex allocation. Princeton University Press, PrincetonGoogle Scholar
  109. Willis BL, Babcock RC, Harrison PL, Oliver JK, Wallace CC (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. In: Proceedings of the 5th International Coral Reef Congress, Tahiti, 1985, vol 4, pp 343–348Google Scholar
  110. Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? Trends Ecol Evol 15:10–13PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.George S. Wise Faculty of Life Sciences, School of ZoologyTel Aviv UniversityTel AvivIsrael

Personalised recommendations