Reproductive biology of the deep brooding coral Seriatopora hystrix: Implications for shallow reef recovery

PLoS ONE

Volumn 12, Issue 5, 2017, Pages

  Prasetia, Rian ^a   Sinniger, Frederic ^a   Hashizume, Kaito ^a   Harii, Saki ^a  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CIRCADIAN RHYTHM; CORAL; CORAL REEF; ECOSYSTEM RESTORATION; HYPOTHESIS; JAPAN; LARVA; MOON; NONHUMAN; ORGANISM COLONY; PLANULA; POLYP (CNIDARIAN); POPULATION DISPERSAL; REPRODUCTION; SEA SURFACE TEMPERATURE; SEASONAL VARIATION; SERIATOPORA HYSTRIX; SHALLOW REEF RECOVERY; TEMPERATURE ACCLIMATIZATION; ANIMAL; ANTHOZOA; ECOSYSTEM; PHYSIOLOGY; SEASON; TEMPERATURE;

SEA WATER;

ANIMALS; ANTHOZOA; CORAL REEFS; ECOSYSTEM; JAPAN; REPRODUCTION; SEASONS; SEAWATER; TEMPERATURE;

EID: 85019571755     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0177034     Document Type: Article

References (86)

1. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, et al. Coral reefs under rapid climate change and ocean acidification. Science. 2007; 318: 1737-1742. https://doi.org/10.1126/science.1152509 PMID: 18079392
2. Hoegh-Guldberg O, Bruno JF. The impact of climate change on the world's marine ecosystem. Science. 2010; 328: 1523-1528. https://doi.org/10.1126/science.1189930 PMID: 20558709
3. Glynn PW. Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol. 1996; 2: 495-509.
4. Riegl B, Piller WE. Possible refugia for reefs in times of environmental stress. Int J Earth Sci. 2003; 92: 520-531.
5. Cacciapaglia C, van Woesik R. Climate-change refugia: shading reef corals by turbidity. Glob Chang Biol. 2016; 22: 1145-1154. https://doi.org/10.1111/gcb.13166 PMID: 26695523
6. Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, et al. Theme section on "Mesophotic Coral Ecosystems: characterization, ecology, and management". Coral Reefs. 2010; 29: 247-251.
7. Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, et al. Community ecology of mesophotic coral reef ecosystems. Coral Reefs. 2010; 29: 255-275.
8. Sinniger F, Morita M, Harii S. "Locally extinct" coral species Seriatopora hystrix found at upper mesophotic depths in Okinawa. Coral Reefs. 2013; 32: 153.
9. Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, et al. Refugia: Identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr. 2012; 21: 393-404.
10. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O. Assessing the "deep reef refugia" hypothesis: Focus on Caribbean reefs. Coral Reefs. 2010; 29: 1-19.
11. Bongaerts P, Riginos C, Brunner R, Englebert N, Smith SR, Hoegh-Guldberg O. Deep reefs are not universal refuges: Reseeding potential varies among coral species. Sci Adv. 2017; 3: e1602373. https://doi.org/10.1126/sciadv.1602373 PMID: 28246645
12. Loya Y, Eyal G, Treibitz T, Lesser MP, Appeldoorn R. Theme section on mesophotic coral ecosystems: advances in knowledge and future perspectives. Coral Reefs. 2016; 35: 1-9.
13. Puglise KA, Colin PL. Understanding mesophotic coral ecosystems: knowledge gaps for management. In: Baker EK, Puglise KA, Harris PT, editors. Mesophotic coral ecosystem-A lifeboat for coral reefs? Nairobi and Arendal: The United Nations Environment Programme and GRID-Arendal; 2016. pp. 83-85.
14. Richmond RH. Energetic relationships and biogeographical differences among fecundity, growth and reproduction in the reef coral Pocillopora damicornis. Bull Mar Sci. 1987; 41: 594-604.
15. Rinkevich B, Loya Y. Variability in the pattern of sexual reproduction of the coral Stylophora pistillata at Eliat, Red Sea: a long-term study. Biol Bull. 1987; 173: 335-344.
16. Vize PD. Deepwater broadcast spawning by Montastraea cavernosa, Montastraea franksi, and Diploria strigosa at the Flower Garden Banks, Gulf of Mexico. Coral Reefs. 2006; 25: 169-171.
17. Holstein DM, Smith TB, Gyory J, Paris CB. Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep. 2015; 5: 12407. https://doi.org/10.1038/srep12407 PMID: 26196243
18. Holstein DM, Smith TB, Paris CB. Depth-independent reproduction in the reef coral Porites astreoides from shallow to mesophotic zones. PLoS One. 2016; 11: e0146068. https://doi.org/10.1371/journal.pone.0146068 PMID: 26789408
19. Eyal-Shaham L, Eyal G, Tamir R, Loya Y. Reproduction, abundance and survivorship of two Alveopora spp. in the mesophotic reefs of Eilat, Red Sea. Sci Rep. 2016; 6: 20964. https://doi.org/10.1038/srep20964 PMID: 26860656
20. Prasetia R, Sinniger F, Harii S. Gametogenesis and fecundity of Acropora tenella (Brook 1892) in a mesophotic coral ecosystem in Okinawa, Japan. Coral Reefs. 2016; 35: 53-62.
21. Harrison PL, Wallace CC. Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z, editor. Ecosystems of the world. Amsterdam: Elsevier Science; 1990. pp. 133-207.
22. Shlesinger Y, Loya Y. Coral Community Reproductive Patterns: Red Sea Versus the Great Barrier Reef. Science. 1985; 228: 1333-1335. https://doi.org/10.1126/science.228.4705.1333 PMID: 17799121
23. Baird AH, Guest JR, Willis BL. Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst. 2009; 40: 551-571.
24. Atoda K. The larva and postlarval development of some reef-building corals. I. Pocillopora damicornis cespitosa (Dana). Sci Reports Tohoku Univ. 1947; 18: 24-47.
25. Atoda K. The larva and postlarval development of some reef-building corals. II. Stylophora pistillata (Esper). Sci Reports Tohoku Univ. 1947; 18: 48-65.
26. Atoda K. The larva and postlarval development of some reef-building corals. V. Seriatopora hystrix. Sci Reports Tohoku Univ. 1951; 19: 33-39.
27. Rinkevich B, Loya Y. The reproduction of the Red Sea coral Stylophora pistillata. II. Synchronization in breeding and seasonality of planulae shedding. Mar Ecol Prog Ser. 1979; 1: 145-152.
28. Harriott VJ. Reproductive seasonality, settlement, and post-settlement mortality of Pocillopora damicornis (Linnaeus), at Lizard Island, Great Barrier Reef. Coral Reefs. 1983; 2: 151-157.
29. Stoddart JA, Black R. Cycles of gametogenesis and planulation in the coral Pocillopora damicornis. Mar Ecol Prog Ser. 1985; 23: 153-164.
30. Dai CF, Soong K, Fan TY. Sexual reproduction of corals in northern and southern Taiwan. Proc 7th Int Coral Reef Symp. 1992; 1: 448-455.
31. Tanner JE. Seasonality and lunar periodicity in the reproduction of Pocilloporid corals. Coral Reefs. 1996; 15: 59-66.
32. de Putron SJ, Smith SR. Planula release and reproductive seasonality of the scleractinian coral Porites astreoides in Bermuda, a high-latitude reef. Bull Mar Sci. 2011; 87: 75-90.
33. McGuire MP. Timing of larval release by Porites astreoides in the northern Florida Keys. Coral Reefs. 1998; 17: 369-375.
34. Richmond RH, Jokiel PL. Lunar periodicity in larva release in the reef coral Pocillopora damicornis at Enewetak and Hawaii. Bull Mar Sci. 1984; 34: 280-287.
35. Villanueva RD, Yap HT, Montaño MNE. Timing of planulation by pocilloporid corals in the northwestern Philippines. Mar Ecol Prog Ser. 2008; 370: 111-119.
36. Isomura N, Nishihira M. Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals. Coral Reefs. 2001; 20: 309-315.
37. Fan TY, Lin K, Kuo F, Soong K, Liu L, Fang L. Diel patterns of larval release by five brooding scleractinian corals. Mar Ecol Prog Ser. 2006; 321: 133-142.
38. Lin CH, Soong K, Fan TY. Hourglass mechanism with temperature compensation in the diel periodicity of planulation of the coral, Seriatopora hystrix. PLoS One. 2013; 8: e64584. https://doi.org/10.1371/journal.pone.0064584 PMID: 23691251
39. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, et al. Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol. 1986; 90: 379-394.
40. Veron JEN. Corals of the world, vol. 2. Townsville: Australian Institute of Marine Science; 2000; p. 48-49.
41. Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kühl M, Muirhead A, et al. Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc R Soc B Biol Sci. 2011; 278: 1840-1850.
42. Nir O, Gruber DF, Einbinder S, Kark S, Tchernov D. Changes in scleractinian coral Seriatopora hystrix morphology and its endocellular Symbiodinium characteristics along a bathymetric gradient from shallow to mesophotic reef. Coral Reefs. 2011; 30: 1089-1100.
43. van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF. The role of deep reefs in shallow reef recovery: An assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol. 2011; 20: 1647-1660. https://doi.org/10.1111/j.1365-294X.2011.05050.x PMID: 21410573
44. Ayre DJ, Resing JM. Sexual and asexual production of planulae in reef corals. Mar Biol. 1986; 90: 187-190.
45. Sherman CDH. Mating system varation in the hermaphroditic brooding coral, Seriatopora hystrix. Heredity. 2008; 100: 296-303. https://doi.org/10.1038/sj.hdy.6801076 PMID: 17987054
46. Warner PA, Willis BL, van Oppen MJH. Sperm dispersal distances estimated by parentage analysis in a brooding scleractinian coral. Mol Ecol. 2016; 25: 1398-1415. https://doi.org/10.1111/mec.13553 PMID: 26818771
47. Stimson JS. Mode and timing of reproduction in some common hermatypic corals of Hawaii and Enewetak. Mar Biol. 1978; 48: 173-184.
48. Yamazato K, Suwardi E, Sultana S. Reproductive cycle of brooding corals at high latitude. J Japanese Coral Reef Soc. 2008; 10: 1-11.
49. Loya K. Sakai K. Yamazato Y. Nakano H. Sambali R. van Woeski Y. Coral bleaching: the winners and the losers. Ecol Lett. 2001; 4: 122-131.
50. van Woesik R, Sakai K, Ganase A, Loya Y. Revisiting the winners and the losers a decade after coral bleaching. Mar Ecol Prog Ser. 2011; 434: 67-76.
51. Sinniger F. Mesophotic coral ecosystems examined: Ryukyu Archipelago, Japan. In: Baker EK, Puglise KA, Harris PT, editors. Mesophotic coral ecosystem-A lifeboat for coral reefs? Nairobi and Arendal: The United Nations Environment Programme and GRID-Arendal; 2016. pp. 43-44.
52. Van Moorsel G. Reproductive strategies in two closely related stony corals (Agaricia, Scleractinia). Mar Ecol Prog Ser. 1983; 13: 273-283.
53. R Core Team. R: A language and environment for statistical computing. 2015. https://www.r-project.org/
54. Rinkevich B. The contribution of photosynthetic products to coral reproduction. Mar Biol. 1989; 101: 259-263.
55. Glynn PW, Gassman NJ, Eakin CM, Cortes J, Smith DB, Guzman HM. Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). I. Pocilloporidae. Mar Biol. 1991; 109: 355-368.
56. Hayashibara T, Shimoike K, Kimura T, Hosaka S, Heyward A, Harrison P, et al. Patterns of coral spawning at Akajima Island, Okinawa, Japan. Mar Ecol Prog Ser. 1993; 101: 253-262.
57. Madsen A, Madin JS, Tan CH, Baird AH. The reproductive biology of the scleractinian coral Plesiastrea versipora in Sydney Harbour, Australia. Sex Early Dev Aquat Org. 2014; 1: 25-33.
58. Harii S, Omori M, Yamakawa H, Koike Y. Sexual reproduction and larval settlement of the zooxanthellate coral Alveopora japonica Eguchi at high latitudes. Coral Reefs. 2001; 20: 19-23.
59. Jokiel PL, Guinther EB. Effects of temperature on the reproduction in the hermatypic coral Pocillopora damicornis. Bull Mar Sci. 1978; 28: 786-789.
60. Fan TY, Li JJ, Ie SX, Fang LS. Lunar periodicity of larval release by pocilloporid corals in Southern Taiwan. Zool Stud. 2002; 41: 288-293.
61. Japan Oceanographic Data Center. Statistics of water temperature and salinity in 1 degree mesh. 2005. http://www.jodc.go.jp/jdoss-stat/stat-infor-sca-e.htm
62. Marshall AT, Clode P. Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs. 2004; 23: 218-224.
63. Jokiel PL, Ito RY, Liu PM. Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis. Mar Biol. 1985; 88: 167-174.
64. Szmant-Froelich A, Reutter M, Riggs L. Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci. 1985; 37: 880-892.
65. Kojis BL. Sexual reproduction in Acropora (Isopora) species (Coelenterata: Scleractinia) - I. A. cuneata and A. palifera on Heron Island reef, Great Barrier Reef. Mar Biol. 1986; 91: 291-309.
66. Zakai D, Dubinsky Z, Avishai A, Caaras T, Chadwick NE. Lunar periodicity of planula release in the reef-building coral Stylophora pistillata. Mar Ecol Prog Ser. 2006; 311: 93-102.
67. Pratchett MS, Gust N, Goby G, Klanten SO. Consumption of coral propagules represents a significant trophic link between corals and reef fish. Coral Reefs. 2001; 20: 13-17.
68. Garcia-Sais JR. Reef habitats and associated sessile-benthic and fish assemblages across a euphotic-mesophotic depth gradient in Isla Desecheo, Puerto Rico. Coral Reefs. 2010; 29: 277-288.
69. Pereira-Filho GH, Amado-Filho GM, Guimarães SMPB Moura RL, Sumida PYG, Abrantes DP, et al. Reef fish and benthic assemblages of the trindade and Martin Vaz island group, SouthWestern Atlantic. Brazilian J Oceanogr. 2011; 59: 201-212.
70. Bryan DR, Kilfoyle K, Gilmore RG, Spieler RE. Characterization of the mesophotic reef fish community in south Florida, USA. J Appl Ichthyol. 2013; 29: 108-117.
71. Kojis BL, Quinn NJ. Seasonal and depth variation in fecundity of Acropora palifera at two reefs in Papua New Guinea. Coral Reefs. 1984; 3: 165-172.
72. Marshall DJ, Keough MJ. The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol. 2008; 53: 1-60.
73. Nozawa Y, Loya Y. Genetic relationship and maturity state of the allorecognition system affect contact reactions in juvenile Seriatopora corals. Mar Ecol Prog Ser. 2005; 286: 115-123.
74. Heyward AJ, Negri AP. Natural inducers for coral larval metamorphosis. Coral Reefs. 1999; 18: 273-279.
75. Putnam HM, Edmunds PJ, Fan TY. Effect of temperature on the settlement choice and photophysiology of larvae from the reef coral Stylophora pistillata. Biol Bull. 2008; 215: 135-142. https://doi.org/10.2307/25470694 PMID: 18840774
76. Ayre DJ, Dufty S. Evidence for restricted gene flow in the viviparous coral Seriatopora hystrix on Australia's Great Barrier Reef. Evolution. 1994; 48: 1183-1201.
77. van Oppen MJH, Lutz A, Glenn D, Peplow L, Kininmonth S. Genetic traces of recent long-distance dispersal in a predominantly self-recruiting coral. PLoS One. 2008; 3: e3401. https://doi.org/10.1371/journal.pone.0003401 PMID: 18852897
78. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP. Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol. 2007; 16: 771-784. https://doi.org/10.1111/j.1365-294X.2006.03187.x PMID: 17284210
79. Maier E, Tollrian R, Rinkevich B, Nurnberger B. Isolation by distance in the scleractinian coral Seriatopora hystrix from the Red Sea. Mar Biol. 2005; 147: 1109-1120.
80. Kahng SE, Copus JM, Wagner D. Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain. 2014; 7: 72-81.
81. Serrano XM, Baums IB, O'Reilly K, Smith TB, Jones RJ, Shearer TL, et al. Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Mol Ecol. 2014; 23: 4226-4240. https://doi.org/10.1111/mec.12861 PMID: 25039722
82. Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC. Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep. 2016; 6: 21619. https://doi.org/10.1038/srep21619 PMID: 26899614
83. Sinniger F, Prasetia R, Yorifuji M, Bongaerts P, Harii S. Seriatopora diversity preserved in upper mesophotic coral ecosystems in Southern Japan. Front Mar Sci. In press.
84. Holstein DM, Paris CB, Vaz AC, Smith TB. Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs. 2016; 35: 23-37.
85. Harii S, Kayanne H. Larval dispersal, recruitment, and adult distribution of the brooding stony octocoral Heliopora coerulea on Ishigaki Island, southwest Japan. Coral Reefs. 2003; 22: 188-196.
86. Hongo C, Kawamata H, Goto K. Catastrophic impact of typhoon waves on coral communities in the Ryukyu Islands under global warming. J Geophys Res. 2012; 117: G02029.