Advertisement

Coral Reproduction in the Eastern Pacific

  • Peter W. GlynnEmail author
  • Susan B. Colley
  • Eugenio Carpizo-Ituarte
  • Robert H. Richmond
Chapter
Part of the Coral Reefs of the World book series (CORW, volume 8)

Abstract

Sexual reproductive activity has been demonstrated in all reef-building (zooxanthellate) scleractinian corals examined from Mexico to the equatorial eastern Pacific (Galápagos Islands). Eleven of 13 species spawn gametes, six are gonochoric, three hermaphroditic, and four exhibit significant mixed sexuality (both gonochoric and hermaphroditic). Four or 30.1 %, two species each of Pocillopora and Porites, produce autotrophic ova. Porites panamensis is the only known zooxanthellate brooder. Also sexually active are the azooxanthellate scleractinian Tubastraea coccinea and the zooxanthellate hydrocoral Millepora intricata. Reproductive structures, sex ratios, age at sexual maturity, sexuality, and developmental mode have been determined from largely histological evidence. Agariciid corals, comprising more than one-third of investigated species, exhibit predominantly mixed sexual systems with sequential cosexual hermaphroditic cycles in four species. Mixed sexuality is also minimally exhibited in populations of two dominantly gonochoric species. Several eastern Pacific corals spawn mostly on lunar day 17 and 1–2 days following; however, multispecific spawning has not been observed probably because of seasonal, diel, and variable timing in spawning behavior. Factors contributing to the high fecundity of eastern Pacific corals include (1) seasonally prolonged reproductive activity, (2) small size of mature gametes allowing for production of high numbers, (3) split spawning with bimonthly gamete production in some species, (4) alternation of sex maturation in gamete development, and possibly (5) their low latitudinal location under relatively constant and high thermal conditions. Coral community persistence, reef growth and recovery are highly dependent on both sexual and asexual reproductive processes. Asexual fragmentation by physical and biotic causes is particularly important, especially for branching pocilloporid species and the fungiid coral Diaseris distorta. Asexual propagation in massive and encrusting poritid and agariciid species is also common-place, often the result of bioerosion and colony breakage by foraging reef fishes. Some research areas in need of attention are noted, for example (a) timing of spawning and the behavior of gamete release of several species, (b) life cycles of Pocillopora spp. and Millepora intricata, and (c) effects of anthropogenic stressors on eastern Pacific coral reproduction and recruitment.

Keywords

Seasonality Broadcast spawning Brooders Fecundity Gametogenesis 

Notes

Acknowledgments

The many individuals who helped with logistics, permitting, collections, histology, and data generation over the years are too numerous to identify here, but are duly acknowledged in the Glynn, Colley et al. publications referenced below. Special thanks go to Bernadette Bezy for sharing information on coral spawning in Costa Rica. This overview benefitted from critiques offered by Joshua S. Feingold and two anonymous reviewers. Information supplied by Peggy Fong, Sascha Steiner and Herman Wirshing is noted with gratitude. We thank Michael C. Schmale for the use of his microscope and digital camera equipment. Joshua Levy and Alissa Mones kindly assisted in producing figures and tables. Principal financial support was provided by grants from the U.S. National Science Foundation (Biological Oceanography Program), the Office of Forestry, Environment and Natural Resources, Bureau for Science and Technology (USAID), the Darwin Initiative (Conservation International), and the National Geographic Society. Essential in-country support has been offered long-term by the Centro de Investigaciones en Ciencias del Mar y Limnología (Costa Rica), the University of Panama, Instituto Nacional de Recursos Naturales, and Smithsonian Tropical Research Institute (Panama), and the Charles Darwin Research Station, Galápagos National Park Service, and Transporte Aereo Militar de Ecuador (Ecuador).

References

  1. Albright R (2011) Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals. J Mar Biol. doi: 10.1155/2011/473615
  2. Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Nat Acad Sci 107:20,400–20,404Google Scholar
  3. Aranceta-Garza F, Balart EF, Reyes-Bonilla H, Cruz-Hernández P (2012) Effect of tropical storms on sexual and asexual reproduction in coral Pocillopora verrucosa subpopulations in the Gulf of California. Coral Reefs 31:1157–1167. doi: 10.1007/s00338-012-0941-9 CrossRefGoogle Scholar
  4. Ayre DJ, Hughes TP, Standish TP (1997) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia. Mar Ecol Prog Ser 159:175–187CrossRefGoogle Scholar
  5. Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141CrossRefGoogle Scholar
  6. Baird AH, Salih A, Trevor-Jones A (2006) Fluorescence census techniques for the early detection of coral recruits. Coral Reefs 25:73–76CrossRefGoogle 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 40:551–571CrossRefGoogle Scholar
  8. Baums IB, Durante MD, Laing AA, Feingold J, Smith T, Bruckner A, Monteiro J (2014) Marginal coral populations: the densest known aggregation of Pocillopora in the Galápagos Archipeligo is of asexual origin. Front Mar Sci 1:59. doi: 10.3389/fmars.2014.00059 CrossRefGoogle Scholar
  9. Bezy MB (2009) Reproducción sexual y reclutamiento del coral masivo, Pavona clavus, en Bahía Culebra, Golfo de Papagayo, Costa Rica. MSc thesis, Univ Costa Rica, San Pedro, Costa Rica, p 151Google Scholar
  10. Birkeland C (1977) The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. In: Proceedings of 3rd International Coral Reef Symposium, vol 1, Miami, pp 15–21Google Scholar
  11. Birkeland C (1997) Geographic differences in ecological processes on coral reefs. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 273–297CrossRefGoogle Scholar
  12. Boulay JN, Cortés J, Nivia-Ruiz J, Baums IB (2012) High genotypic diversity of the reef-building coral Porites lobata (Scleractinia: Poritidae) in Isla del Coco National Park, Costa Rica. Rev Biol Trop (suppl 3):279–292Google Scholar
  13. Boulay JN, Hellberg ME, Cortés J, Baums IB (2013) Unrecognized coral species diversity masks differences in functional ecology. Proc R Soc B 281:20131580. doi: 10.1098/rspb.2013.1580 CrossRefGoogle Scholar
  14. Boumeester J, Berumeni ML, Baird AH (2011) Daytime broadcast spawning of Pocillopora verrucosa on coral reefs of the central Red Sea, Galaxea. J Coral Reef Stud 13:23–24CrossRefGoogle Scholar
  15. Cabral-Tena RA, Reyes-Bonilla H, Lluch-Cota S, Paz-García DA, Calderón-Aguilera LE, Norzagaray-López O, Balart EF (2013) Different calcification rates in males and females of the coral Porites panamensis in the Gulf of California. Mar Ecol Prog Ser 476:1–8CrossRefGoogle Scholar
  16. Campos-Vázquez RA, Balart EF, Vallejo-Fuerte M, Rodríguez-Jaramillo C (2014). Ciclo reproductivo de los corales Pocillopora verrucosa y Pocillopora meandrina en Isla Gaviota, Bahía de La Paz, Mexico. Congr Nac Oceanogr June 2014. La Paz, MexicoGoogle Scholar
  17. Carpizo-Ituarte E, Vizcaíno-Ochoa V, Chi-Barragán G, Tapia-Vázquez O, Cupul-Magaña AL, Medina-Rosas P (2011) Evidence of sexual reproduction in the hermatypic corals Pocillopora damicornis, Porites panamensis, and Pavona gigantea in Banderas Bay, Mexican Pacific. Cienc Mar 37:97–112Google Scholar
  18. Charnov EL (1982) The theory of sex allocation. Princeton monographs in population biology 18. Princeton Univ Press, Princeton NJ, p 355Google Scholar
  19. Chávez-Romo E, Reyes-Bonilla H (2007) Sexual reproduction of the coral Pocillopora damicornis in the southern Gulf of California, Mexico. Cienc Mar 33:495–501Google Scholar
  20. Cohen AI, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanisms. Oceanogr 22:118–127CrossRefGoogle Scholar
  21. Colley SB, Feingold JS, Peña J, Glynn PW (2000) Reproductive ecology of Diaseris distorta (Michelin) (Fungiidae) in the Galápagos Islands, Ecuador. In: Proceedings of 9th International Coral Reef Symposium, vol 1, Bali, pp 373–379Google Scholar
  22. Colley SB, Glynn PW, May AS, Maté JL (2006) Species-dependent reproductive responses of eastern Pacific corals to the 1997–1998 ENSO event. In: Proceedings of 10th International Coral Reef Symposium, vol 1, Okinawa, pp 61–70Google Scholar
  23. Combosch DJ, Vollmer SV (2011) Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the tropical eastern Pacific. PLoS ONE 6(8):e21200. doi: 10.1371/journal.pone.0021200 CrossRefGoogle Scholar
  24. Connolly SR, Baird AH (2010) Estimating dispersal potential for marine larvae: dynamic models applied to scleractinian corals. Ecology 91:3572–3583CrossRefGoogle Scholar
  25. Cortés J, Jiménez C (2003) Corals and coral reefs of the Pacific of Costa Rica: history, research and status. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 361–385CrossRefGoogle Scholar
  26. Cox EF (2007) Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 26:721–724CrossRefGoogle Scholar
  27. Dana TF (1975) Development of contemporary eastern Pacific coral reefs. Mar Biol 33:355–374CrossRefGoogle Scholar
  28. D’Croz L, Robertson DR (1997) Coastal oceanographic conditions affecting coral reefs on both sides of the Isthmus of Panama. In: Proceedings of 8th International Coral Reef Symposium, vol 2, Panama, pp 2053–2058Google Scholar
  29. Done TJ, Potts DC (1992) Influences of habitat and natural disturbances on contributions of massive Porites corals to reef communities. Mar Biol 114:479–493CrossRefGoogle Scholar
  30. Edmunds PJ (2010) Population biology of Porites astreoides and Diploria strigosa on a shallow Caribbean reef. Mar Ecol Prog Ser 418:87–104CrossRefGoogle Scholar
  31. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Poll Bull 50:125–146CrossRefGoogle Scholar
  32. Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals: a review. Coral Reefs 2:129–150CrossRefGoogle Scholar
  33. Feingold JS (1995) Effects of elevated water temperature on coral bleaching and survival during El Niño disturbance events. Ph.D. dissert, Univ of Miami, Coral Gables, Florida p 236Google Scholar
  34. Fenner D (2001) Biogeography of three Caribbean corals (Scleractinia) and the invasion of Tubastraea coccinea into the Gulf of Mexico. Bull Mar Sci 69:1175–1189Google Scholar
  35. Fenner D, Banks K (2004) Orange cup coral Tubastraea coccinea invades Florida and the Flower Garden Banks, northwestern Gulf of Mexico. Coral Reefs 23:505–507Google Scholar
  36. Figueira de Paula AF, Creed JC (2004) Two species of the coral Tubastraea (Cnidaria, Scleractinia) in Brazil: a case of accidental introduction. Bull Mar Sci 74:175–183Google Scholar
  37. Fine D, Tehernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811(single page)Google Scholar
  38. Fong P, Glynn PW (2001) Population abundance and size-structure of an eastern tropical Pacific reef coral after the 1997–98 ENSO: a simulation model predicts field measures. Bull Mar Sci 69:187–202Google Scholar
  39. Fong P, Smith TB, Wartian MJ (2006) Epiphytic cyanobacteria maintain shift to macroalgal dominance on coral reefs following ENSO disturbance. Ecology 87:1162–1168CrossRefGoogle Scholar
  40. Fukami H, Chen CA, Budd AF, Collins A, Wallace C, Chuang Y-Y, Chen C, Dai C-F, Iwao K, Sheppard C, Knowlton N (2008) Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoS ONE 3:1–9CrossRefGoogle Scholar
  41. García-Ocampo MR (2005) Patrones de reclutamiento de las colonias juveniles de coral del género Pocillopora Lamarck 1816 (Anthozoa: Scleractinia) en cinco localidades de Ixtapa-Zihuatanejo, Guerrero, México. Undergrad thesis Mar Biol, Univ del Mar, Pto Ángel, Oaxaca p 56Google Scholar
  42. Garren M, Walsh SM, Caccone A, Knowlton N (2006) Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 25:503–512CrossRefGoogle Scholar
  43. Giese AC, Pearse JS (1974) Introduction: general principles. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates, vol 1. Academic Press, New York, pp 1–49Google Scholar
  44. Glynn PW (1984) Widespread coral mortality and the 1982–83 El Niño warming event. Environ Conserv 11:133–146CrossRefGoogle Scholar
  45. Glynn PW (1985) El Niño-associated disturbance to coral reefs and post disturbance mortality by Acanthaster planci. Mar Ecol Prog Ser 26:295–300CrossRefGoogle Scholar
  46. Glynn PW (1990) Coral mortality and disturbances to coral reefs in the tropical eastern Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Niño-Southern Oscillation. Elsevier Oceanogr Ser 52, Amsterdam, Elsevier, pp 55–126Google Scholar
  47. Glynn PW (2003) Coral communities and coral reefs of Ecuador. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 449–472CrossRefGoogle Scholar
  48. Glynn PW (2008) Food-web structure and dynamics of eastern tropical Pacific coral reefs: Panamá and Galápagos Islands. In: McClanahan TR, Branch GM (eds) Food webs and the dynamics of marine reefs. Oxford Univ Press, Oxford, pp 185–208CrossRefGoogle Scholar
  49. Glynn PW, Ault JS (2000) A biogeographic analysis and review of the far eastern Pacific coral reef region. Coral Reefs 19:1–23CrossRefGoogle Scholar
  50. Glynn PW, Colley SB (2008) Survival of brooding and broadcasting reef corals following large scale disturbances: is there any hope for broadcasting species during global warming? In: Proceedings of 11th International Coral Reef Symposium. Ft Lauderdale (session 11), pp 1–5Google Scholar
  51. Glynn PW, Fong P (2006) Patterns of reef coral recovery by the regrowth of surviving tissues following the 1997–98 El Niño warming and 2000, 2001 upwelling cool events in Panamá, eastern Pacific. In: Proceedings of 10th International Coral Reef Symposium, vol 1, Okinawa, pp 624–630Google Scholar
  52. Glynn PW, Stewart RH, McCosker JE (1972) Pacific coral reefs of Panamá: structure, distribution and predators. Geol Rundsch 61:483–519CrossRefGoogle Scholar
  53. Glynn PW, Peters EC, Muscatine L (1985) Coral tissue microstructure and necrosis: relation to catastrophic coral mortality in Panamá. Dis Aquat Org 1:29–37CrossRefGoogle Scholar
  54. Glynn PW, Gassman NJ, Eakin CM, Cortés J, Smith DB, Guzmán HM (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá, and Galápagos Islands (Ecuador) I. Pocilloporidae. Mar Biol 109:355–368CrossRefGoogle Scholar
  55. Glynn PW, Colley SB, Eakin CM, Smith DB, Cortés J, Gassman NJ, Guzmán HM, Del Rosario JB, Feingold JB (1994) Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá, and Galápagos Islands (Ecuador) II. Poritidae. Mar Biol 118:191–208CrossRefGoogle Scholar
  56. Glynn PW, Colley SB, Gassman NJ, Black K, Cortés J, Maté JL (1996) Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá, and Galápagos Islands (Ecuador). III. Agariciidae (Pavona gigantea and Gardineroseris planulata). Mar Biol 125:579–601Google Scholar
  57. Glynn PW, Colley SB, Ting JH, Maté JL, Guzmán HM (2000) Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá, and Galápagos Islands (Ecuador). IV. Agariciidae, recruitment and recovery of Pavona varians and Pavona sp a. Mar Biol 136:785–805CrossRefGoogle Scholar
  58. Glynn PW, Maté JL, Stemann TA (2001a) Pavona chiriquiensis, a new species of zooxanthellate scleractinian coral (Cnidaria: Anthozoa: Agariciidae) from the eastern tropical Pacific. Bull Biol Soc Wash 10:210–225Google Scholar
  59. Glynn PW, Maté JL, Baker AC, Calderón MO (2001b) Coral bleaching and mortality in Panamá and Ecuador during the 1997–1998 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109Google Scholar
  60. Glynn PW, Colley SB, Maté JL, Cortés J, Guzmán HM, Bailey RL, Feingold JS, Enochs IC (2008) Reproductive ecology of the azooxanthellate coral Tubastraea coccinea in the equatorial eastern Pacific: Part V. Dendrophylliidae. Mar Biol 153:529–544CrossRefGoogle Scholar
  61. Glynn PW, Colley SB, Guzmán HM, Enochs IC, Cortés J, Maté JL, Feingold J (2011) Reef coral reproduction in the eastern Pacific: Costa Rica, Panamá and the Galápagos Islands (Ecuador). VI. Agariciidae, Pavona clavus. Mar Biol 158:1601–1617CrossRefGoogle Scholar
  62. Glynn PW, Colley SB, Maté JL, Baums IB, Feingold JS, Cortés J, Guzmán HM, Afflerbach JC, Brandtneris VW, Ault JS (2012) Reef coral reproduction in the equatorial eastern Pacific: Costa Rica, Panamá, and the Galápagos Islands (Ecuador). VII Siderastreidae, Psammocora stellata and Psammocora profundacella. Mar Biol 159:1,917–1,932 doi: 10.1007/s00227-012-1979-5
  63. Golbuu Y, Richmond RH (2007) Substratum preferences in planula larvae of two species of scleractinian corals, Goniastraea retiformis and Stylarea punctata. Mar Biol 152:639–644CrossRefGoogle Scholar
  64. Graham EM, Baird AH, Connolly SR (2008) Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27:529–539CrossRefGoogle Scholar
  65. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631CrossRefGoogle Scholar
  66. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189CrossRefGoogle Scholar
  67. Guest JR, Baird AH, Goh BPL, Chou LM (2005) Seasonal reproduction in equatorial coral reefs. Inv Repr Dev 48:207–218CrossRefGoogle Scholar
  68. Guest JR, Baird AH, Goh BPL, Chou LM (2012) Sexual systems in scleractinian corals: an unusual pattern in the reef-building species Diploastrea heliopora. Coral Reefs. doi: 10.1007/s00338-012-0881-4 Google Scholar
  69. Guzmán HM (1986) Estructura de la comunidad arrecifal de la Isla del Caño, Costa Rica, y el efecto de perturbaciones naturales severas. MSc thesis, Univ Costa Rica, San Pedro, Costa Rica, p 179Google Scholar
  70. Guzmán HM (1988) Distribución y abundancia de organismos coralívoros en los arrecifes coralinos de la Isla del Caño, Costa Rica. Rev Biol Trop 36:191–207Google Scholar
  71. Guzmán HM, Cortés J (1989) Coral reef community structure at Caño Island, Pacific Costa Rica. Publ Staz zool Napoli (I: Mar Ecol) 10:23–41Google Scholar
  72. Guzmán HM, Cortés J (2001) Changes in reef community structure after fifteen years of natural disturbances in the eastern Pacific (Costa Rica). Bull Mar Sci 69:133–149Google Scholar
  73. Guzmán HM, Cortés J (2007) Reef recovery 20 years after the 1982–1983 El Niño massive mortality. Mar Biol 151:401–411CrossRefGoogle Scholar
  74. Hanafy MH, Aamer MA, Habib M, Rouphael AB, Baird AH (2010) Synchronous reproduction of corals in the Red Sea. Coral Reefs 29:119–124CrossRefGoogle Scholar
  75. Harriott VJ (1983) Reproductive ecology of four scleractinian species at Lizard Island, Great Barrier Reef. Coral Reefs 2:9–18CrossRefGoogle Scholar
  76. Harrison PL (1990) Sperm morphology and fertilization strategies in scleractinian corals. Adv Invert Reprod 5:299–304Google Scholar
  77. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Berlin, pp 59–85CrossRefGoogle Scholar
  78. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs, ecosystems of the world 25. Elsevier, Amsterdam, pp 133–207Google Scholar
  79. Highsmith RC (1980) Geographic patterns of coral bioerosion: a productivity hypothesis. J Exp Mar Biol Ecol 46:177–196CrossRefGoogle Scholar
  80. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226CrossRefGoogle Scholar
  81. Hirose M, Hidaka M (2000) Reduced reproductive success in scleractinian corals that survived the 1998 bleaching in Okinawa. Galaxea JCRS 2:17–21CrossRefGoogle Scholar
  82. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough J, Marshall P, Nystrom M, Palumbi SR, Pandolphi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefGoogle Scholar
  83. Humason GL (1967) Animal tissue techniques, 2nd edn. WH Freeman and Co, San Francisco, p 569Google Scholar
  84. Humphrey C, Weber M, Lott C, Cooper T, Fabricius K (2008) Effects of suspended sediments, dissolved inorganic nutrients and salinity on fertilization and embryo development in the coral Acropora millepora (Ehrenberg, 1834). Coral Reefs 27:837–850Google Scholar
  85. Jiménez CE (1996–1997) Coral colony fragmentation by whitetip reef sharks at Coiba Island National Park, Panamá. Rev Biol Trop 44/45:698–700Google Scholar
  86. Jiménez CE (1998) Arrecifes y comunidades coralinas de Bahía Culebra, Pacífico norte de Costa Rica (Golfo de Papagayo). MSc thesis, Univ Costa Rica, San Pedro, Costa Rica, p 218Google Scholar
  87. Kerr AM (2005) Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony. Biol Rev 80:543–558CrossRefGoogle Scholar
  88. Kinzie RA III (1993) Spawning in the reef corals Pocillopora verrucosa and P. eydouxi at Sesoko Island, Okinawa. Galaxea 11(2):93–105Google Scholar
  89. Kleypas JA, McManus JW, Meñez LAB (1999) Environmental limits to coral reef development: where do we draw the line? Amer Zool 39:146–159CrossRefGoogle Scholar
  90. Kolinski SP, Cox EF (2003) An update on modes and timing of gamete and planula release in Hawaiian scleractinian corals with implications for conservation and management. Pac Sci 57:17–27CrossRefGoogle Scholar
  91. LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, López Pérez A, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc B 277:2925–2934CrossRefGoogle Scholar
  92. Lewis JB (2006) Biology and ecology of the hydrocoral Millepora on coral reefs. Adv Mar Biol 50:1–55CrossRefGoogle Scholar
  93. Lirman D, Glynn PW, Baker AC, Leyte Morales GE (2001) Combined effects of three sequential storms on the Huatulco coral reef tract, Mexico. Bull Mar Sci 69:267–278Google Scholar
  94. López-Pérez RA, Mora-Pérez MG, Leyte-Morales GE (2007) Coral (Anthozoa: Scleractinia) recruitment at Bahías de Huatulco, western México: implications for coral community structure and dynamics. Pac Sci 61:355–369CrossRefGoogle Scholar
  95. Loya Y, Sakai K (2008) Bidirectional sex change in mushroom stony corals. Proc R Soc B 275:2335–2343CrossRefGoogle Scholar
  96. Loya Y, Sakai K, Heyward A (2009) Reproductive patterns of fungoid corals in Okinawa, Japan, Galaxea. J Coral Reef Stud 11:119–129CrossRefGoogle Scholar
  97. Luna JG (1968) Manual of histological staining methods of the armed forces institute of pathology. McGraw-Hill, New YorkGoogle Scholar
  98. Mangubhai S, Harrison PL (2009) Extended breeding seasons and asynchronous spawning among equatorial reef corals in Kenya. Mar Ecol Prog Ser 374:305–310CrossRefGoogle Scholar
  99. Manzello DP (2010) Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs 29:749–758CrossRefGoogle Scholar
  100. Manzello DP, Kleypas JA, Budd DA, Eakin CM, Glynn PW, Langdon C (2008) Poorly cemented coral reefs of the eastern tropical Pacific: possible insights into reef development in a high-CO2 world. Proc Nat Acad Sci 105:10,450–10,455Google Scholar
  101. Maté JL (2003) Corals and coral reefs of the Pacific coast of Panamá. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 387–417CrossRefGoogle Scholar
  102. Medina-Rosas P, Carriquiry JD, Cupul-Magaña AL (2005) Recruitment of Porites (Scleractinia) on artificial substrate in reefs affected by the 1997–98 El Niño in Banderas Bay, Mexican Pacific. Cienc Mar 31:1–7Google Scholar
  103. Mundy CN (2000) An appraisal of methods used in coral recruitment studies. Coral Reefs 19:124–131CrossRefGoogle Scholar
  104. Oliver J, Babcock R (1992) Aspects of the fertilization ecology of broadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. Biol Bull 183:409–417CrossRefGoogle Scholar
  105. Oliver JK, Babcock RC, Harrison PL, Willis BL (1988) Geographic extent of mass coral spawning: clues to ultimate causal factors. In: Proceedings of 6th International Coral Reef Symposium, vol 2, Townsville, pp 803–810Google Scholar
  106. Omori M, Fukami H, Kobinata H, Hatta M (2001) Significant drop of fertilization of Acropora corals in 1999: an after effect of heavy coral bleaching? Limnol Oceanogr 46:704–706Google Scholar
  107. Penland L, Kloulechad J, Idip D, van 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
  108. Peters EC, Gassman NJ, Firman JC, Richmond RH, Power EA (1997) Ecotoxicology of tropical marine ecosystems. J Environ Tox Chem, Annu Rev 16:12–40CrossRefGoogle Scholar
  109. Pinzón JH, Reyes-Bonilla H, Baums IB, LaJeunesse TC (2012) Contrasting clonal structures among Pocillopora (Scleractinia) communities at two environmentally distinct sites in the Gulf of California. Coral Reefs. doi: 10.1007/s00338-012-0887-4 Google Scholar
  110. Reyes-Bonilla H (1993) Estructura de la comunidad, influencia de la depredación y biología poblacional de corales hermatípicos en el arrecife de Cabo Pulmo, B.C.S. MSc thesis, Centro de Investigación Científica y de Educación Superior de Ensenada, Depart Ecología, p 169Google Scholar
  111. Reyes-Bonilla H (2002) Checklist of valid names and synonyms of stony corals (Anthozoa: Scleractinia) from the eastern Pacific. J Nat Hist 36:1–13CrossRefGoogle Scholar
  112. Reyes-Bonilla H (2003) Coral reefs of the Pacific coast of Mexico. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 331–349CrossRefGoogle Scholar
  113. Reyes-Bonilla H, Calderón-Aguilera LE (1994) Parámetros poblacionales de Porites panamensis (Anthozoa: Scleractinia), en el arrecife de Cabo Pulmo, México. Rev Biol Trop 42:121–128Google Scholar
  114. Richmond RH (1985) Variations in the population biology of Pocillopora damicornis across the Pacific. In: Proceedings of 5th International Coral Reef Congress, vol 6, Tahiti, pp 101–106Google Scholar
  115. Richmond RH (1987a) Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533CrossRefGoogle Scholar
  116. 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
  117. Richmond RH (1988) Competency and dispersal potential of planula larvae of a spawning versus a brooding coral. In: Proceedings of 6th International Coral Reef Symposium, vol 2, Townsville, pp 827–831Google Scholar
  118. Richmond RH (1990) The effects of the El Niño/Southern Oscillation on the dispersal of corals and other marine organisms. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Niño-Southern Oscillation. Elsevier Oceanogr Ser 52, Amsterdam, Elsevier, pp 127–140Google Scholar
  119. Richmond RH (1993) Coral reefs: present problems and future concerns resulting from anthropogenic disturbance. Am Zool 33:524–536CrossRefGoogle Scholar
  120. Richmond RH (1994) Effects of coastal runoff on coral reproduction. In: Ginsburg RN (compiler) Proceedings of the colloquium on global aspects of coral reefs: health, hazards and history. Rosenstiel School of Marine and Atmospheric Science, Univ Miami, Miami, pp 360–364Google Scholar
  121. 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 175–197CrossRefGoogle Scholar
  122. Richmond RH (2005) Coral reproduction and recruitment as tools for studying the ecotoxicology of coral reef ecosystems. In: Ostrander G (ed) Techniques in aquatic toxicology, vol II. CRC Press, Boca Raton, Florida, pp 331–338Google Scholar
  123. 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 60:185–203CrossRefGoogle Scholar
  124. Rinkevich B (1989) The contribution of photosynthetic products to coral reproduction. Mar Biol 101:259–263CrossRefGoogle Scholar
  125. Rodríguez-Troncoso AP (2004) Caracterización del ciclo reproductivo de Pocillopora damicornis (Linnaeus 1758), en el arrecife de la Entrega, Oaxaca, México. Undergrad thesis, Univ del Mar, Pto Ángel, Oaxaca, p 62Google Scholar
  126. 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 158:2673–2683CrossRefGoogle Scholar
  127. Romano SL, Palumbi SR (1996) Evolution of scleractinian corals inferred from molecular systematics. Science 271:640–642CrossRefGoogle Scholar
  128. Sammarco PW (1982) Polyp bail-out: an escape response to environmental stress and a new means of reproduction in corals. Mar Ecol Prog Ser 10:57–65Google Scholar
  129. Santiago Valentín JD, Rodríguez-Troncoso AP, Carpizo-Ituarte E, Benítez-Villalobos F, Torres-Hernández P, López-Pérez A (2015) Reproductive pattern of the reef building coral Pavona gigantea (Scleractinia: Agariciidae) off southwestern Mexico. Cienc Mar 41:233–246Google Scholar
  130. Schmidt-Roach S, Miller KJ, Woolsey E, Gerlach G, Baird AH (2012) Broadcast spawning by Pocillopora species on the Great Barrier Reef. PLoS ONE 7(12):e50847. doi: 10.1371/journal.pone.0050847 CrossRefGoogle Scholar
  131. Scott PJB, Risk MJ (1988) The effect of Lithophaga (Bivalvia: Mytilidae) boreholes on the strength of the coral Porites lobata. Coral Reefs 7:145–151CrossRefGoogle Scholar
  132. Shlesinger Y, Loya J (1985) Coral community reproductive patterns: Red Sea versus the Great Barrier Reef. Science 228:1333–1335CrossRefGoogle Scholar
  133. Shlesinger Y, Goulet TL, Loya Y (1998) Reproductive patterns of scleractinian corals in the northern Red Sea. Mar Biol 132:691–701CrossRefGoogle Scholar
  134. Smith DB (1991) The reproduction and recruitment of Porites panamensis Verrill at Uva Island, Pacific Panamá. MS thesis, Univ Miami, Coral Gables, Florida, p 64Google Scholar
  135. Smith TB, Glynn PW, Maté JL, Toth LT, Gyory J (2014) A depth refugium from catastrophic coral bleaching prevents regional extinction. Ecology 95:1663–1673. doi: 10.1890/13-0468.1 CrossRefGoogle Scholar
  136. Soong K, Cho LC (1998) Synchronized release of medusa from three species of hydrozoan fire corals. Coral Reefs 17:145–154CrossRefGoogle Scholar
  137. Steiner SCC, Cortés J (1996) Spermatozoan ultrastructure of scleractinian corals from the eastern Pacific: Pocilloporidae and Agariciidae. Coral Reefs 15:143–147CrossRefGoogle Scholar
  138. Strathmann RR, Hughes TP, Kuris AM, Lindeman KC, Morgan SG, Pandolfi JM, Warner RR (2002) Evolution of local recruitment and its consequences for marine populations. Bull Mar Sci 70(suppl):377–396Google Scholar
  139. Szmant-Froelich A, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892Google Scholar
  140. Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54CrossRefGoogle Scholar
  141. Szmant AM, Gassman NL (1990) The effects of prolonged ‘bleaching’ on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224CrossRefGoogle Scholar
  142. Tomascik T, Sander F (1987) Effects of eutrophication on reef-building corals III. Reproduction of the reef-building coral Porites porites. Mar Biol 94:77–94CrossRefGoogle Scholar
  143. van Veghel MLJ (1993) Multiple species spawning on Curaçao reefs. Bull Mar Sci 52:1017–1021Google Scholar
  144. van Woesik R (2009) Calm before the spawn: global coral spawning patterns are explained by regional wind fields. Proc R Soc B 277:715–722CrossRefGoogle Scholar
  145. Waller RG, Taylor PA, Gage JD (2005) Sexual reproduction in three hermaphroditic deep-sea Caryophyllia species (Anthozoa: Scleractinia) from the NE Atlantic Ocean. Coral Reefs 24:594–602Google Scholar
  146. Ward S, Harrison P, Hoegh-Guldberg O (2000) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. In: Proceedings of 9th International Coral Reef Symposium, vol 2, Bali, pp 1123–1128Google Scholar
  147. Wartian MJ (2006) Determinants of community structure and resilience on tropical eastern Pacific coral reefs. PhD dissert, Univ Calif, Los Angeles, p 247Google Scholar
  148. Wellington GM (1982) Depth zonation of corals in the Gulf of Panama: control and facilitation by resident reef fishes. Ecol Monogr 52:223–241CrossRefGoogle Scholar
  149. Willis BL, Babcock RC, Harrison PL, Wallace CC (1993) Experimental evidence of hybridization in reef corals involved in mass spawning events. In: Proceedings of 7th International Coral Reef Symposium, vol 1, Guam, p 504 (abstract)Google Scholar
  150. Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006) The role of hybridization in the evolution of reef corals. Annu Rev Ecol Evol Syst 37:489–517CrossRefGoogle Scholar
  151. Wilson JR, Harrison PL (2003) Spawning patterns of scleractinian corals at the Solitary Islands—a high latitude coral community in eastern Australia. Mar Ecol Prog Ser 260:115–123CrossRefGoogle Scholar
  152. Yamashiro H, Nishihira M (1998) Experimental study of growth and asexual reproduction in Diaseris distorta (Michelin 1843) a free-living fungoid coral. J Exp Mar Biol Ecol 225:253–267CrossRefGoogle Scholar
  153. Zapata FA, Vargas-Ángel B (2003) Corals and coral reefs of the Pacific coast of Colombia. In: Cortés J (ed) Latin American coral reefs. Elsevier, Amsterdam, pp 419–447CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Peter W. Glynn
    • 1
    Email author
  • Susan B. Colley
    • 2
  • Eugenio Carpizo-Ituarte
    • 3
  • Robert H. Richmond
    • 4
  1. 1.Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  2. 2.Stanley S. Scott Cancer CenterLSU Health Science Center New OrleansNew OrleansUSA
  3. 3.Laboratorio de Ecología y Biología Del DesarrolloInstituto de Investigaciones Oceanológicas, Universidad Autónoma de Baja CaliforniaBaja CaliforniaMexico
  4. 4.Kewalo Marine LaboratoryUniversity of Hawaii at ManoaHonoluluUSA

Personalised recommendations