Embryogenesis and larval biology of the cold-water coral Lophelia pertusa

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Larsson, Ann I ^a   Järnegren, Johanna ^b   Strömberg, Susanna M ^a   Dahl, Mikael P ^a,e   Lundälv, Tomas ^c   Brooke, Sandra ^d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b NORWEGIAN INSTITUTE FOR NATURE RESEARCH   (Norway)

^c GÖTEBORG UNIVERSITY   (Sweden)

^d FLORIDA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; ATLANTIC OCEAN; CORAL REEF; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION; LARVAL DEVELOPMENT; LONGEVITY; LOPHELIA PERTUSA; MALE; NEMATOCYST; NONHUMAN; PLANULA; POPULATION DISPERSAL; SPAWNING; SPECIES HABITAT; SURVIVAL RATE; SWIMMING; ANIMAL; ANIMAL BEHAVIOR; ANTHOZOA; BIOLOGICAL MODEL; COLD; EMBRYOLOGY; GENETIC MARKER; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; PHYSIOLOGY; REPRODUCTION;

DNA; GENETIC MARKER; WATER;

ANIMALS; ANTHOZOA; ATLANTIC OCEAN; BEHAVIOR, ANIMAL; COLD TEMPERATURE; DNA; EMBRYONIC DEVELOPMENT; GENETIC MARKERS; LARVA; MODELS, BIOLOGICAL; REPRODUCTION; SWIMMING; WATER;

EID: 84904302180     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102222     Document Type: Article

References (97)

1. Rogers AD (1999) The biology of Lophelia pertusa (Linneus, 1758) and other deep-water reef-forming corals and impacts from human activities. Int Rev Hydrobiol 84:315-406
2. Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543-547
3. Roberts JM, Wheeler A, Freiwald A, Cairns S (2009) Cold-Water Corals. The Biology and Geology of Deep-Sea Coral Habitats. Cambridge, UK
4. Cordes EE, McGinley MP, Podowski EL (2008) Coral Communities of the deep Gulf of Mexico. Deep Sea Research I 55:777-787
5. Henry L-A, Roberts JM (2007) Biodiversity and ecological composition of macrobenthos on cold water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep Sea Research I 54: 654-672 (Pubitemid 46528261)
6. Mortensen PB, Hovland M, Brattegard T, Farestveit R (1995) Deep water bioherms of the scleractinian coral Lophelia pertusa (L.) at 64o N on the Norwegian shelf: structure and associated megafauna. Sarsia 80: 145-158 (Pubitemid 3004784)
7. Williams B, Risk MJ, Ross SW, Sulak KJ (2006) Deep-water antipatharians: Proxies of environmental change. Geology 34:773-776. (Pubitemid 44430764)
8. Roark BE, Guilderson TP, Dunbar RB, Fallon SJ, Mucciarone DA, et al. (2009) Extreme longevity in proteinaceous deep-sea corals. Proc Nat Acad Sci 106(13): 5204-5208
9. Rogers AD (1994) The biology of seamounts. Adv Mar Biol 30:305-350
10. Davies AJ, Roberts MJ, Hall-Spencer J (2007) Preserving deep-sea natural heritage: emerging issues in offshore conservation and management. Biol Conserv 138:299-312 (Pubitemid 47187304)
11. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: Open or closed? Science 287:857-859 (Pubitemid 30084329)
12. Waller RG (2005) Deep-water Scleractinia (Cnidaria: Anthozoa): current knowledge of reproductive processes. In: Cold-water corals and ecosystems. Freiwald A, Roberts JM (eds) Springer-Verlag, New York, pp 691-700
13. Kerr AM, Baird AH, Hughes TP (2010) Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia). P R Soc B 278:75-81
14. Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals. A review. Coral Reefs 2:129-150
15. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Coral Reefs: An ecosystem in transition. Dubinsky Z, Stambler N (eds) Springer Science+ Business Media B.V.,Dordrecht, pp 59-85
16. Brooke S, Järnegren J (2013) Reproductive periodicity of the scleractinian coral Lophelia pertusa from the Trondheim Fjord, Norway. Mar Biol 160:139-153
17. Waller RG, Tyler PA, Smith CR (2008) Fecundity and embryo development of three Antarctic deep-water scleractinians: Flabellum thouarsii, F. curvatum and F. impensum. Deep-Sea Res Pt II 55:2527-2534
18. Mercier A, Sun Z, Hamel J-F (2011) Reproductive periodicity, spawning and development of the deep-sea scleractinian coral Flabellum angulare. Mar Biol 158:371-380
19. Reed JK (1980) Distribution and structure of deep-water Oculina varicosa coral reefs off central eastern Florida. B Mar Sci 30:667-677
20. Brooke S, Young CM (2003) Reproductive ecology of a deep-water scleractinian coral, Oculina varicosa, from the southeast Florida shelf. Cont Shelf Res 23:847-858 (Pubitemid 36751283)
21. Brooke S, Young CM (2005) Embryogenesis and larval biology of the ahermatypic scleractinian Oculina varicosa. Mar Biol 146:665-675 (Pubitemid 40383656)
22. Waller RG, Tyler PA (2005) The reproductive biology of two deep-water, reef-building scleractinians from the NE Atlantic Ocean. Coral Reefs 24:514-522 (Pubitemid 41738387)
23. Brooke S (in press) Reproductive biology of deep-sea corals. Ch. 10 In: Demopoulos AWJ, Ross SW, Kellogg CA, Morrison CL, Nizinski M, et al. Deepwater Program: Lophelia II Continuing Ecological Research on Deep-Sea Corals and Deep Reef Habitat in the Gulf of Mexico. US Geological Survey Report.
24. Jackson JBC (1986) Modes of dispersal of clonal benthic invertebrates: consequences for species' distributions and genetic structure of local populations. B Mar Sci 39:588-606
25. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol-Prog Ser 7:207-226
26. Rosen BR, Taylor JD (1969) Reef coral from Aldabra - New mode of reproduction. Science 166:119-121
27. Sammarco PW (1982) Polyp Bail-Out: An escape response to environmental stress and a new means of reproduction in corals. Mar Ecol-Prog Ser 10:57-65
28. Stoddart JA (1983) Asexual production of planulae in the coral Pocillopora damicornis. Mar Biol 76:279-284
29. Ayre DJ, Resing JM (1986) Sexual and asexual production of planulae in reef corals. Mar Biol 90:187-190
30. Ayre DJ, Hughes TP, Standish RS (1997) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia. Mar Ecol-Prog Ser 159:175-187 (Pubitemid 28034835)
31. 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
32. Heyward AJ, Negri AP (2012) Turbulence, cleavage, and the naked embryo: A case for coral clones. Science 335: 1064
33. Dahl MP, Pereyra RT, Lundälv T, André C (2012) Fine-scale spatial genetic structure and clonal distribution of the cold-water coral Lophelia pertusa. Coral Reefs 31:1135-1148
34. Martin VJ, Koss R (2002) Phylum Cnidaria. Atlas of marine invertebrate larvae. 51-108
35. Tranter PRG, Nicholson DN, Kinchington D (1982) A description of spawning and post-gastrula development of the cool temperate coral, Caryophyllia smithii. J Mar Biol Ass UK 62:845-854
36. Raimondi PT, Morse ANC (2000). The consequences of complex larval behavior in a coral. Ecology 81: 3193-3211.
37. Ritson-Williams R, Arnold S, Fogarty N, Steneck RS, Vermeij MJA, et al. (2009). New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci38: 437-457.
38. Stake JL, Sammarco PW (2003) Effects of pressure on swimming behavior in planula larvae of the coral Porites astreoides (Cnidaria, Scleractinia). J Exp Mar Biol Ecol 288:181-201 (Pubitemid 36400075)
39. Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273-279 (Pubitemid 29478088)
40. Baird AH, Morse ANC (2004) Induction of metamorphosis in larvae of the brooding corals Acropora palifera and Stylopora pistillata. Mar Freshwater Res 55:469-472 (Pubitemid 39234841)
41. Webster NS, Smith LD, Heyward AJ, Watts JEM, Webb RI, et al. (2004) Metamorphosis of a Scleractinian coral in response to microbial biofilms. Appl Environ Microb 70:1213-1221 (Pubitemid 38568251)
42. Birrell CL, McCook LJ, Willis BL, Harrington L (2008) Chemical effects of macroalgae on larval settlement of the broadcast spawning coral Acropora millepora. Mar Ecol-Prog Ser 362:129-137 (Pubitemid 352045318)
43. Gleason DF, Danilowicz BR, Nolan CJ (2009) Reef waters stimulate substratum exploration in planulae from brooding Caribbean corals. Coral Reefs 28:549-554
44. Harii S, Kayanne H (2002) Larval settlement of corals in flowing water using a racetrack flume. Mar Technol Soc J 36:76-79
45. Altieri AH (2003) Settlement cues in the locally dispersing temperate cup coral Balanophyllia elegans. Biol Bull 204:241-245
46. Le Goff-Vitry MC, Pybus OG, Rogers AD (2004) Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Mol Ecol 13:537-549 (Pubitemid 38260938)
47. Morrison CL, Ross SW, Nizinski MS, Brooke S, Järnegren J, et al. (2011) Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean. Conserv Genet 12:713-729
48. Bell N, Smith J (1999) Coral growing on North Sea oil rigs. Nature 402:601
49. Roberts JM (2002) The occurrence of the coral Lophelia pertusa and other conspicuous epifauna around an oil platform in the North Sea. Underwater Technol 25: 83-91
50. Gass SE, Roberts JM (2006) The occurrence of the cold-water coral Lophelia pertusa (Scleractinia) on oil and gas platforms in the North Sea: colony growth, recruitment and environmental controls on distribution. Mar Pollut Bull 52:549-559 (Pubitemid 43767502)
51. Johnson MS, Black R (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol 70:157-164
52. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443-466
53. White C, Selkoe KA, Watson J, Siegel DA, Zacheri DC, et al. (2010) Ocean currents help explain population genetic structure. Proceedings of the Royal Society B: Biological Sciences 277: 1685-1694
54. Fiksen Ø, Jørgensen C, Kristiansen T, Vikebø F, Huse G (2007) Linking behavioural ecology and oceanography: larval behaviour determines growth, mortality and dispersal. Mar Ecol-Prog Ser 347:195-205 (Pubitemid 350124701)
55. Connolly SR, Baird AH (2010) Estimating dispersal potential for marine larvae: dynamic models applied to scleractinian corals. Ecology 91:3572-3583
56. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with Image J. Biophotonics International July Issue: 7pp
57. Chinga-Carrasco G (2002) Microscopy and computerized image analysis of wood pulp fibres multi-scale structures. In: Méndez-Vilas A, Díaz J (Eds) Microscopy: Science, Technology, Applications and Education, Formatex, Badajoz, pp 2182-2189
58. Larsson AI, Lundälv T, van Oevelen D (2013) Skeletal growth, respiration rate and fatty acid composition in the cold-water coral Lophelia pertusa under varying food conditions. Mar Ecol-Prog Ser 483:169-184
59. Wisshak M, Freiwald A, Lundälv T, Gektidis M (2005) The physical niche of the bathyal Lophelia pertusa in a non-bathyal setting: environmental controls and palaeoecological implications. 979-1001. In: Cold-water corals and ecosystems. JM FAR, Springer-Verlag Berlin Heidelberg.
60. Wagner H, Purser A, Thomsen L, Jesus CC, Lundalv T (2011) Particulate organic matter fluxes and hydrodynamics at the Tisler cold-water coral reef. Journal of Marine Systems 85:19-29
61. Morrison CL, Eackles MS, Johnson RL, King TL (2008) Characterization of 13 microsatellite loci for the deep-sea coral, Lophelia pertusa (Linnaeus 1758), from the western North Atlantic Ocean and Gulf of Mexico. Mol Ecol Resour 8:1037-1039
62. Mangubhai S, Harrison PL (2009) Extended breeding seasons and asynchronous spawning among equatorial reef corals in Kenya. Mar Ecol-Prog Ser 374:305-310
63. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, et al. (1984) Mass spawning in tropical reef corals. Science 223:1186-1189 (Pubitemid 15271586)
64. 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 183:409-417 (Pubitemid 24406259)
65. Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, et al. (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. Evolution 58:308-323 (Pubitemid 38362376)
66. Neulinger SC, Järnegren J, Ludvigsen M, Lochte K, Dullo WC (2008) Phenotype-specific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral's nutrition, health, and distribution. Appl Environ Microb 74:7272-7285 (Pubitemid 352773607)
67. Levin LA, Bridges TS (1995) Pattern and diversity in reproduction and development. In: Ecology of Marine Invertebrate Larvae. McEdward LR (ed), CRC Press, Boca Raton, pp 1-48
68. Brusca RC, Brusca GJ (2003) Invertebrates, 2nd edition. Chapter 8: Phylum Cnidaria 219-268. Sinauer Associates, Sunderland
69. Szmant-Froelich A, Yevich P, Pilson MEQ (1980) Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa, Scleractinia). Biol Bull 158:257-269
70. Strathmann MF (1987) Phylum Cnidaria, class Anthozoa. In: Reproduction and development of marine invertebrates of the northern Pacific coast. Strathmann MF, University of Washington Press, pp 83-104
71. Ball EE, Hayward DC, Reece-Hoyes JS, Hislop NR, Samuel G, et al. (2002) Coral development: from classical embryology to molecular control. Int J Dev Biol 46:671-678 (Pubitemid 36841036)
72. Chia F-S, Crawford B (1973) Some observations on gametogenesis, larval development and substratum selection of the sea pen Ptilosarcus guerneyi. Mar Biol 23:73-82
73. Valentine JW (1997) Cleavage patterns and the topology of the metazoan tree of life. PNAS 94:8001-8005
74. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745-749 (Pubitemid 351522763)
75. Martindale MQ (2005) The evolution of metazoan axial properties. Nat Rev Genet 6:917-927
76. Hayashibara T, Ohike S, Kakikinuma Y (1997) Embryonic and larval development and planula metamorphosis of four gamete-spawning Acropora (Anthozoa, Scleractinia). Proceedings of the 8th International Coral Reef Symposium, Panama 2: 1231-1236
77. Hayward DC, Miller DJ, Ball EE (2004) snail expression during embryonic development of the coral Acropora: blurring the diploblast/triploblast divide? Dev Genes Evol 214:257-260 (Pubitemid 38801521)
78. Yamashita K, Kawaii S, Nakai M, Fusetani N (2003) Larval behavioral, morphological changes, and nematocyte dynamics during settlement of actinulae of Tubularia mesembryanthemum, Allman 1871 (Hydrozoa : Tubulariidae). Biol Bull 204:256-269 (Pubitemid 36738203)
79. Chia F-S, Koss R (1979) Fine structural studies of the nervous system and the apical organ in the planula larva of the sea anemone Anthopleura elegantissima. J Morphol 160:275-298
80. Rentzsch F, Fritzenwanker JH, Scholz CB, Technau U (2008) FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 135:1761-1769
81. Gleason DF, Hofmann DK (2011) Coral larvae: From gametes to recruits. J Exp Mar Biol Ecol 408:42-57
82. Lavaleye MSS, Duineveld GCA (2001) Coral recruitment experiments. ACES Deliverable 20 5 pp.
83. Thiem Ø, Ravagnan E, Fosså JH, Berntsen J (2006) Food supply mechanisms for cold-water coral along a continental shelf edge. J Marine Syst 60:207-219
84. Davies AJ, Duineveld GCA, Lavaleye MSS, Bergman MJN, van Haren H, et al. (2009) Downwelling and deep-water bottom currents as food supply mechanisms to the cold-water coral Lophelia pertusa (Scleractinia) at the Mingulay Reef complex. Limnol Oceanogr 54:620-629
85. Larsson AI, Jonsson PR (2006) Barnacle larvae actively select flow environments supporting post-settlement growth and survival. Ecology 87:1960-1966 (Pubitemid 44215720)
86. Lavaleye M, Duineveld G, Lundälv T, Guihen D, Kiriakoulakis K, et al. (2009) Cold-water corals on the Tisler reef: preliminary observations on the dynamic reef envrionment. Oceanography 22:76-84
87. Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, et al. (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341-375 (Pubitemid 34696169)
88. Mullineaux LS, Mills SW (1997) A test of the larval retention hypothesis in seamount-generated flows. Deep-Sea Res 44:745-770
89. Dullo W-C, Flögel S, Rüggeberg A (2008) Cold-water coral growth in relation to the hydrography of the Celtic and Nordic European continental margin. Mar Ecol-Prog Ser 371:165-176
90. Stoddart JA, Babcock RC, Heyward AJ (1988) Self-fertilization and maternal enzymes in the planulae of the coral Goniastrea favulus. Mar Biol 99:489-494
91. Hellberg ME, Taylor MS (2002) Genetic analysis of sexual reproduction in the dendrophylliid coral Balanophyllia elegans. Mar Biol 141:629-637 (Pubitemid 36072718)
92. Baums IB, Hughes CR, Hellberg ME (2005) Mendelian microsatellite loci for the Caribbean coral Acropora palmata. Mar Ecol-Prog Ser 288:115-127 (Pubitemid 40554677)
93. Smith KL, Alberts SC, Bayes MK, Bruford MW, Altmann J, et al. (2000) Cross-species amplification, non-invasive genotyping, and non-mendelian inheritance of human STRPs in Savannah baboons. Am J Primatol 51:219-227 (Pubitemid 30613353)
94. Dobrowolski MP, Tommerup IC, Blakeman HD, O'Brien PA (2002) Non-mendelian inheritance revealed in a genetic analysis of sexual progeny of Phytophthora cinnamomi with mircosatellite markers. Fungal Genet Biol 35:197-212
95. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol lett 9:615-629
96. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522-527 (Pubitemid 43157730)
97. Corell H, Moksnes PO, Engqvist A, Döös K, Jonsson PR (2012) Depth distribution of larvae critically affects their dispersal and the efficiency of marine protected areas. Mar Ecol-Prog Ser 467:29-46