How Corals Coordinate and Organize: An Ecosystemic Analysis Based on Biocommunication and Fractal Properties

Chapter

Abstract

Tropical coral reefs harbour some of the most diverse biological communities on our planet and as such rival tropical forests communities in species diversity and number of individuals from all domains. The cooperative interplay of prokaryotes, eukaryotes – particularly – the interactions among plantae and animalia shape this delicate balance, which ultimately culminate in the beauty of the coral reef biome. Some algal species but especially scleractinian corals with their interconnected organizational structure precipitate a calcium-carbonate skeleton that, upon generation after generation, form and shape structures that can even be seen from space. Yet this process is limited by light penetrability – either by depth or by visibility – that provides endosymbiotic algae with the energetic flux to convert light quanta into biochemically available energy. As a result, the sheer dominance of coral species somewhat camouflages the delicate balance between reef builders and bioerosive processes. This intrinsically interwoven biocommunicative dynamics is a key issue in order to comprehend how such structures can evolve and stretch out over 1,000s of km. Neglecting the importance of these processes compromises a full understanding of reef-dynamics and in turn promotes accelerated reef degradation due to improper use of reef resources to those who rely on them. Doing so simply increments reef instability and as such its long-term survival. This article attempts to shed light on the crucial role of biocommunicative processes and how these are manifested across taxa. In fact biocommunication is so essential in assigning each organism a specific role in this network of interdependences that the elegance even within organisms themselves – seen from a biomic perspective –attain self-similar properties. In turn and regardless of the taxa involved, self-similarity in coral reef ecosystems is an underlying feature that relies on intact and efficient biocommunicative pathways.

References

  1. Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, Beltran-Ramirez V, Miller DJ, Wiedenmann J, Salih A, Mats MV (2008) Diversity and evolution of coral fluorescent proteins. PLoS One 3(7):e2680 1–12Google Scholar
  2. Alker AP, Kim K, Dube DH et al (2004) Localized induction of a generalized response against multiple biotic agents in Caribbean sea fans. Coral Reef 23:397–405Google Scholar
  3. Ates R (1989) Aggressive behavior in corals. FAMA 12:104–112Google Scholar
  4. Baird AH, Bhagooli R, Ralph PJ et al (2009) Coral bleaching. The role of the host. Trends Ecol Evol 24:16–20PubMedGoogle Scholar
  5. Bak RPM, Termaat RM, Dekker R (1982) Complexity of coral interactions; influence of time, location of interaction and epifauna. Mar Biol 69:215–222Google Scholar
  6. Barnes R, Hughes R (1999) An introduction to marine ecology, 3rd edn. Blackwell Science, OxfordGoogle Scholar
  7. Basillais E (1998) Functional role of the fractal morphology of corals: a full model of the nutrient turbulent diffusion fluxes to a coral reef. C R Acad Sci Paris Sci de la vie 321:295–298Google Scholar
  8. Begon M, Harper JL, Townsend CR (1996) Ecology, individuals, populations and communities, 3rd edn. Blackwell Science, OxfordGoogle Scholar
  9. Bigger CH, Olano CT (1993) Alloimmune cellular responses of the gorgonian coral Swiftia exserta. J Immunol 150:134Google Scholar
  10. Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta 1760:1690–1695PubMedGoogle Scholar
  11. Bradbury H, Reichelt RE (1983) Fractal dimension of a coral reef at ecological scales. Mar Ecol Prog Ser 10:169–171Google Scholar
  12. Bruno JF, Witman JD (1996) Defense mechanisms of scleractinian cup corals against overgrowth by colonial invertebrates. J Exp Mar Biol Ecol 207:229–241Google Scholar
  13. Buddemeier R, Baker A, Fautin DG et al (2004) The adaptive hypothesis of bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin/HeidelbergGoogle Scholar
  14. Chadwick-Furman N, Rinkevich B (1994) A complex allorecognition system in a reef-building coral: delayed responses, reversals and nontransitive hierarchies. Coral Reef 13:57–63Google Scholar
  15. Chaumette A, Chaumette G (2008) Beyond the blue. Liquid Motion Film, USAGoogle Scholar
  16. Chen CA, Wallace CC, Yu JK et al (2000) Strategies for amplification by polymerase chain reaction of the complete sequence of the gene encoding nuclear large subunit ribosomal RNA in corals. Mar Biotechnol 2:558–570PubMedGoogle Scholar
  17. Chen MC, Cheng YM, Hong MC et al (2004) Molecular cloning of Rab5 (ApRab5) in Aiptasia pulchella and its retention in phagosomes harboring live zooxanthellae. Biochem Biophys Res Commun 324:1024–1033PubMedGoogle Scholar
  18. Chen MC, Hong MC, Huang YS et al (2005) ApRab11, a cnidarian homologue of the recycling regulatory protein Rab11, is involved in the establishment and maintenance of the Aiptasia-Symbiodinium endosymbiosis. Biochem Biophys Res Commun 338:1607–1616PubMedGoogle Scholar
  19. Connell JH (1976) Competitive interactions and the species diversity of corals. In: Mackie GO (ed) Coelenterate ecology and behavior. Plenum Press, New YorkGoogle Scholar
  20. Cope M (1982) Interspecific coral interactions in Hong Kong. Proc 4th Int Coral Reef Symp Manila 2:357–362Google Scholar
  21. Edmunds PJ, Gates RD (2003) Has coral bleaching delayed our understanding of fundamental aspects of coral–dinoflagellate symbioses? BioScience 53:976–980Google Scholar
  22. Elmqvist T, Folke C, Nyström M et al (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488–494Google Scholar
  23. Enquist BJ, Niklas KJ (2001) Invariant scaling relations across tree-dominated communities. Nature 410:655–660PubMedGoogle Scholar
  24. Enquist BJ, Brown JH, West GB (1998) Allometric scaling of plant energetics and population density. Nature 395:163–165Google Scholar
  25. Enquist BJ, Haskell JP, Tiffney BH (2002) General patterns of taxonomic and biomass partitioning in extant and fossil plant communities. Nature 419:610–613PubMedGoogle Scholar
  26. Ferriz-Dominguez N, Horta-Puga G (2001) Short-term aggressive behavior in scleractinian corals from La Blanquilla reef, Ve-racruz reef system. Rev Biol Trop 49:67–75PubMedGoogle Scholar
  27. Frank U, Rinkevich B (2001) Alloimmune memory is absent in the Red Sea hydrocoral Millepora dichotoma. J Exp Zool 291:25–39PubMedGoogle Scholar
  28. Geffen Y, Rosenberg E (2005) Stress-induced rapid release of antibacterials by scleractinian corals. Mar Biol 146:931–935Google Scholar
  29. Geistner J (1977) The influence of wave exposure on the ecological zonation of Caribbean coral reefs. Proc 3rd Int Coral Reef Symp Miami 2:23–29Google Scholar
  30. Gleason DF, Edmunds PJ, Gates RD (2005) Ultraviolet radiation effects on the behavior and recruitment of larvae from the reef coral Porites astreoides. Mar Biol 148:503–512Google Scholar
  31. Golberg K, Eltzov E, Shnit-Orland M, Marks RS, Kushmaro A (2011) Characterization of quorum sensing signals in coral-associated bacteria. Microb Ecol 61:783–792PubMedGoogle Scholar
  32. Gunthorpe L, Cameron AM (1990) Toxic exudates from the hard coral Goniopora tenuidens. Toxicon 28:1347–1350PubMedGoogle Scholar
  33. Hallock P (1997) Reefs and reef limestones in earth history. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, LondonGoogle Scholar
  34. Harrison PL, Babcock RC, Bull GD et al (1984) Mass spawning in tropical reef corals. Science 223:1186–1189PubMedGoogle Scholar
  35. Hatcher BG (1997) Organic production and decomposition. In: Birkeland C (ed) Life and death of coral reefs. Chapman & Hall, LondonGoogle Scholar
  36. Hay ME (1997) The ecology and evolution of seaweed-herbivore interactions on coral reefs. Coral Reef 16:67–76Google Scholar
  37. Hay ME, Fenical W, Gustafson K (1987) Chemical defense against diverse coral-reef herbivores. Ecology 68:1581–1591Google Scholar
  38. Hidaka M, Yurugi K, Sunagawa S et al (1997) Contact reactions between young colonies of the coral Pocillopora damicornis. Coral Reef 16:13–20Google Scholar
  39. Hildemann WH, Raison RL, Cheung G et al (1977) Immunological specificity and memory in a scleractinian coral. Nature 270:219–223PubMedGoogle Scholar
  40. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866Google Scholar
  41. Hoegh-Guldberg O (2004) Coral reefs and projections of future change. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin/HeidelbergGoogle Scholar
  42. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedGoogle Scholar
  43. Horiguchi T, Kawai H, Kubota M et al (1999) Phototactic responses of four marine dinoflagellates with different types of eye-spot and chloroplast. Phycol Res 47:101–107Google Scholar
  44. Hughes TP (1994) Catastrophes, phase-shifts and large scale degradation of a Caribbean coral reef. Science 265:1547–1551PubMedGoogle Scholar
  45. Idjadi JA, Karlson RH (2007) Spatial arrangement of competitors influences coexistence of reef-building corals. Ecology 88:2449–2454PubMedGoogle Scholar
  46. Iguchi K, Kukaya T, Yasumoto A et al (2004) New marine sesquiterpenoids and diterpenoids from the Okinawan soft coral Cla-vularia koellikeri. J Nat Prod 67:577–583PubMedGoogle Scholar
  47. Iwashima M, Matsumoto Y, Takahashi H, Iguchi K (2000) New marine steroids, yonarasterols, isolated from the okinawan soft coral, Clavularia viridis. Steroids 65(3):130–137PubMedGoogle Scholar
  48. Iwao K, Fujisawa T, Hatta M (2002) A cnidarian neuropeptide of the GLW-amide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reef 21:127–129Google Scholar
  49. Jones AM, Berkelmans R, van Oppen MJ et al (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc Biol Sci 275:1359–1365PubMedGoogle Scholar
  50. Kelman D, Benayahu Y, Kashman Y (1999) Chemical defence of the soft coral Parerythropodium fulvum fulvum (Forskal) in the Red Sea against generalist reef fish. J Exp Mar Biol Ecol 238:127–137Google Scholar
  51. Kelman D, Kashman Y, Rosenberg E, Kushmaro A, Loya Y (2006) Antimicrobial activity of Red Sea corals. Mar Biol 149:357–363Google Scholar
  52. Kelmanson IV, Matz MV (2003) Molecular basis and evolutionary origins of color diversity in great star coral Montastraea cavernosa (Scleractinia: Faviida). Mol Biol Evol 20:1125–1133PubMedGoogle Scholar
  53. Kenkel CD, Traylor MR, Wiedenmann J, Salih A, Matz VM (2011) Fluorescence of coral larvae predicts their settlement response to crustose coralline algae and reflects stress. Proc R Soc B 278:2691–2697PubMedGoogle Scholar
  54. Kim K (1994) Antimicrobial activity in gorgonian corals (Coe-lenterata, Octocorallia). Coral Reef 13:75–80Google Scholar
  55. Kiselev VG, Hahn KR, Auer DP (2003) Is the brain cortex a fractal? NeuroImage 20:1765–1774PubMedGoogle Scholar
  56. Koblinger L, Hofmann W (1985) Analysis of human lung morphometric data for stochastic aerosol deposition calculations. Phys Med Biol 30:541–556PubMedGoogle Scholar
  57. Koblinger L, Hofmann W (1988) Stochastic morphometric model of the rat lung. Anat Rec 221:533–539PubMedGoogle Scholar
  58. Koh EGL (1997) Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23:379–398Google Scholar
  59. Kramarsky-Winter E (2004) What can regeneration process tell us about coral disease? In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin/HeidelbergGoogle Scholar
  60. Krediet CJ, Ritchie KB, Paul VJ, Teplitski M (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc R Soc B 280(20122328):1–9Google Scholar
  61. Kushmaro A, Kramarsky-Winter E (2004) Bacteria as a source of coral nutrition. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin/HeidelbergGoogle Scholar
  62. Lang JC (1970) Inter-specific aggression within the scleractinian reef corals. PhD thesis, Yale University, New HavenGoogle Scholar
  63. Lang JC (1971) Interspecific aggression by scleractinian corals; 1. The rediscovery of Scolymia cubensis (Milne-Edwards and Haime). Bull Mar Sci 21:952–959Google Scholar
  64. Lang JC (1973) Interspecific aggression by scleractinian corals. Why the race is not only to the swift. Bull Mar Sci 23:260–279Google Scholar
  65. Lang JC, Chornesky EA (1990) Competition between scleractinian reef corals – a review of mechanisms and effects. In: Dubinsky Z (ed) Coral reefs; ecosystems of the world 25. Elsevier, AmsterdamGoogle Scholar
  66. Leruste A, Bouvier T, Bettarel Y (2012) Enumerating viruses in coral mucus. Appl Environ Microbiol 78(17):6377–6379PubMedGoogle Scholar
  67. Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252Google Scholar
  68. Leutenegger A, D’Angelo C, Matz MV, Denzel A, Oswald F, Salih A, Nienhaus GU, Wiedenmann J (2007) It’s cheap to be colourful – Anthozoans show a slow turnover of GFP-like proteins. FEBS 274:2496–2505Google Scholar
  69. Lindquist N, Hay ME (1996) Palatability and chemical defense of marine invertebrate larvae. Ecol Monogr 66:431–450Google Scholar
  70. Logan A (1986) Aggressive behavior in reef corals: a strategy for survival. Sea Front 32:347–351Google Scholar
  71. Madl P, Antonius A, Kleemann K (2005) The silent sentinels – the demise of tropical coral reefs. BUFUS 32–34. Available online: http://biophysics.sbg.ac.at/reefs/reefs.htm. Accessed March 2013
  72. Madl P, Egot-Lemaire S (2013) The field and the photon from a physical point of view (Ch.2); Detection and measurement of photonic emissions of biogenic origin (Ch.3). In: Fels D, Cifra M (eds) Fields of the cell (in press)Google Scholar
  73. Madl P, Hofmann W, Oldham MJ, Asgharian B (2010) Stochastic morphometric model of the Balb/c mouse lung. Anat Rec 293:1766–1775Google Scholar
  74. Margulis L, Schwartz KV (1988) Five kingdoms. W. H. Freeman and Company, New YorkGoogle Scholar
  75. Marhaver KL, Edwards RA, Rohwer F (2008) Viral communities associated with healthy and bleaching corals. Environ Microbiol 10:2277–2286PubMedGoogle Scholar
  76. Márquez LM, van Oppen MJH, Willis BL et al (2002) Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and Acropora cytherea are genetically distinct. Proc Natl Acad Sci U S A 269:1289–1294Google Scholar
  77. Martin KC (2004) Local protein synthesis during axon guidance and synaptic plasticity. Curr Opin Neurobiol 14:305–310PubMedGoogle Scholar
  78. Matz MV, Marshall NJ, Vorobyev M (2006) Are corals colorful? Photochem Photobiol 2006(82):345–350Google Scholar
  79. Mazel CH (2004) Fluorescent enhancement of signalling in a mantis shrimp. Science 303:51PubMedGoogle Scholar
  80. McClanahan TR, Maina J (2003) Response of coral assemblages to the interaction between natural temperature variation and rare warm-water events. Ecosystems 6:551–563Google Scholar
  81. Miller KJ, Ayre DJ (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92:557–568PubMedGoogle Scholar
  82. Miller DJ, van Oppen MJH (2003) A ‘fair go’ for coral hybridisation. Mol Ecol 12:805–807PubMedGoogle Scholar
  83. Moccia R, Chen D, Lyles V et al (2003) An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J Neurosci 23:9409–9417PubMedGoogle Scholar
  84. Mora C, Aburto-Oropeza O, Ayala Bocos A, Ayotte PM, Banks S et al (2011a) Global human footprint on the linkage between biodiversity and ecosystem functioning in reef fishes. PLoS Biol 9(4):1–9Google Scholar
  85. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B (2011b) How many species are there on earth and in the ocean? PLoS Biol 9(8):1–8Google Scholar
  86. Mumby PJ, Edwards AJ, Arias-Gonzales JE et al (2004) Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427:533–536PubMedGoogle Scholar
  87. Mydlarz LD, Holthouse SF, Peters EC et al (2008) Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. PLoS ONE 3(3): e1811 1–9Google Scholar
  88. Netea MG, Quintin J, van der Meer JWM (2011) Trained immunity: a memory for innate host defense. Cell Host Microbe 9(5):355–361PubMedGoogle Scholar
  89. Neulinger SC, Järnegren J, Ludvigsen M et al (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 Microbiol 74:7272–7285PubMedGoogle Scholar
  90. Okubo N, Motokawa T, Okubo N et al (2007) Embryogenesis in the reef-building coral Acropora spp. Zool Sci 24:1169–1177PubMedGoogle Scholar
  91. Palmer CV, Modi CK, Mydlarz LD (2009) Coral fluorescent proteins as antioxidants. PLoS One 4(10):e7298 1–9Google Scholar
  92. Penland L, Loulechad J, Idip D et al (2004) Coral spawning in the western Pacific Ocean is related to solar insolation: evidence of multiple spawning events in Palau. Coral Reef 23:133–140Google Scholar
  93. Purkis SJ, Riegl BM, Dodge RE (2006) Fractal patterns of coral communities: evidence from remote sensing (Arabian Gulf, Dubai, UAE). In: Proceedings of the 10th international coral reef symposium, Okinawa, 28 June–2 July 2004, pp 1753–1762, accessed: Aug. 2013: http://www.nova.edu/ocean/forms/sam_purkis_fractal_patterns_coral.pdf
  94. Ramesh P, Venkateswarlu Y (1999) Novel steroid constituents of the soft coral Sinularia dissecta. Steroids 64:785–789PubMedGoogle Scholar
  95. Rinkevich B (2004) Allorecognition and xenorecognition in reef corals: a decade of interactions. Hydrobiologia 530(531):443–450Google Scholar
  96. Rinkevich B, Sakai K (2001) Interspecific interactions among species of the coral genus Porites from Okinawa. Jpn J Zool 104:91–97Google Scholar
  97. Rinkevich B, Frank U, Bak RPM et al (1994) Alloimmune responses between Acropora hemprichi conspecifics: nontransitive patterns of overgrowth and delayed cytotoxicity. Mar Biol 118:731–737Google Scholar
  98. Rohwer F (2010) Coral reefs in the microbial seas. Plaid Press Productions, Oakdale. http://www.nova.edu/ocean/forms/sam_purkis_fractal_patterns_coral.pdf. Accessed August 2013
  99. Rohwer F, Kelley S (2004) Culture-independent analyses of coral-associated microbes. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin/HeidelbergGoogle Scholar
  100. Rosenberg E (2004) The bacterial disease hypothesis of coral bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin/HeidelbergGoogle Scholar
  101. Rosenberg E, Kushmaro A, Kramarsky-Winter E et al (2009) The role of microorganisms in coral bleaching. ISME J 3:139–146PubMedGoogle Scholar
  102. Roussis V, Chinou IB, Tsitsimpikou C et al (2001) Antibacterial secondary metabolites antibacterial activity of volatile secondary metabolites from Caribbean soft corals of the genus Gorgonia. Flavour Fragr J 16:364–366Google Scholar
  103. Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430:742PubMedGoogle Scholar
  104. Rozenblat YBH, Rosenberg E (2004) Temperature-regulated bleaching and tissue lysis of Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin/HeidelbergGoogle Scholar
  105. Ryan FP (2006) Genomic creativity and natural selection: a modern synthesis. Biol J Linn Soc 88:655–672Google Scholar
  106. Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 48(2000):850–853Google Scholar
  107. Sampayo EM, Ridgway T, Bongaerts P et al (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449PubMedGoogle Scholar
  108. Santos SR, Taylor DJ, Kinzie A et al (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111PubMedGoogle Scholar
  109. Shackelton LA, Holmes EC (2004) The evolution of large DNA viruses: combining genomic information of viruses and their hosts. Trends Microbiol 12:458–465PubMedGoogle Scholar
  110. Sharon G, Rosenberg E (2008) Bacterial growth on coral mucus. Curr Microbiol 56:481–488PubMedGoogle Scholar
  111. Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380PubMedGoogle Scholar
  112. Slattery M, James A, McClintock JB, Heine JN (1995) Chemical defenses in Antarctic soft corals: evidence for antifouling compounds. J Exp Mar Biol Ecol 190:61–77Google Scholar
  113. Slattery M, Hines GA, Starmer J et al (1999) Chemical signals in gametogenesis, spawning, and larval settlement and defense of the soft coral Sinularia polydactyla. Coral Reef 18:75–84Google Scholar
  114. Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. UNEP-WCMC and University of California Press, Los AngelesGoogle Scholar
  115. Stambler N, Dubinsky Z (2005) Corals as light collectors: an integrating sphere approach. Coral Reef 24:1–9Google Scholar
  116. Stat M, Morris E, Gates RD (2008) Functional diversity in coral– dinoflagellate symbiosis. Proc Natl Acad Sci U S A 105:9256–9261PubMedGoogle Scholar
  117. Takabayashia M, Santos CR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164Google Scholar
  118. Tanner JE (1997) Interspecific competition reduces fitness in scleractinian corals. J Exp Mar Biol Ecol 214:19–34Google Scholar
  119. Thompson KR, Otis KO, Chen DY et al (2004) Synapse to nucleus signaling during long-term synaptic plasticity: a role for the classical active nuclear import pathway. Neuron 44:997–1009PubMedGoogle Scholar
  120. Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of Montastraea annularis species complex: patterns of distribution of four taxa of symbiodinium on different reefs and across depths. Biol Bull 201:348–359PubMedGoogle Scholar
  121. Twan WH, Hwang JS, Chang CF (2003) Sex steroids in scleratinian coral, Euphyllia ancora: implication in mass spawning. Biol Reprod D 68:2255–2260Google Scholar
  122. Twan WH, Hwang JS, Lee YH et al (2006) Hormones and re-production in scleractinian corals. Comp Biochem Physiol A Mol Integr Physiol 144:247–253PubMedGoogle Scholar
  123. Van Oppen JH, McDonald BJ, Willis B et al (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol Biol Evol 18:1315–1329PubMedGoogle Scholar
  124. Van Oppen M, Leong JA, Gates RD (2009) Coral-virus interaction: a double-edged sword? Symbiosis 47:1–8Google Scholar
  125. Van Veghel MLJ, Cleary DFR, Bak RPM (1996) Interspecific interactions and competitive ability of the polymorphic reef-building coral Montastrea annularis. Bull Mar Sci 58:792–803Google Scholar
  126. van Woesik R (2009) Calm before the spawn: global coral spawning patterns are explained by regional winds fields. Proc R Soc B 1524:1–8Google Scholar
  127. Vargas-Angel B, Colley SB, Hoke SM et al (2006) The reproductive seasonality and gametogenic cycle of Acropora cervicornis off Broward County, Florida, USA. Coral Reef 25:110–122Google Scholar
  128. Veron JEN (1986) Corals of Australia and the Indo-Pacific. University of Hawaii Press, HonoluluGoogle Scholar
  129. Veron JEN (1995) Corals in space and time – the biogeography and evolution of the Scleractinia. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  130. Veron JEN, Stafford-Smith M (2000) Corals of the world, vol 3. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  131. Villarreal LP (2005) Viruses and the evolution of life. ASM Press, Washington, DCGoogle Scholar
  132. Vytopil E, Willis B (2001) Epifaunal community structure in Acropora spp. (Scleractinia) on the Great Barrier reef: implications of coral morphology and habitat complexity. Coral Reef 20:281–288Google Scholar
  133. Watanabe K, Sekine M, Iguchi K (2003) Isolation of three marine prostanoids, possible biosynthetic intermediates for clavulones, from the Okinawan soft coral Clavularia viridis. Pharm Bull 51:909–913Google Scholar
  134. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. Exp Biol 211:3059–3066Google Scholar
  135. Weis VM, Reynolds WS, deBoer MD et al (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reef 20:301–308Google Scholar
  136. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126PubMedGoogle Scholar
  137. Westfall JA, Sayyar KL (1997) Ultrastructure of neurons and synapses in the tentacle epidermis of the sea anemone Calliactis parasitica. J Morphol 232:207–216PubMedGoogle Scholar
  138. Wilsanand V, Wagh AB, Bapuji M (1999) Antibacterial activities of anthozoan corals on some marine microfoulers. Microbios 99:137–145PubMedGoogle Scholar
  139. Witzany G (2010) Biocommunication and natural genome editing. Springer, DordrechtGoogle Scholar
  140. Witzany G (ed) (2011) Biocommunication in soil microorganisms. Springer, Heidelberg/New YorkGoogle Scholar
  141. Witzany G (ed) (2012) Biocommunication of fungi. Springer, DordrechtGoogle Scholar
  142. Witzany G, Baluska F (eds) (2012) Biocommunication of plants. Springer, Heidelberg/BerlinGoogle Scholar
  143. Yamazato K, Yeemin T (1986) Preliminary study on the inter- and intraspecific interactions among corals of Khang Khao Island, the Sichang Islands, Gulf of Thailand. Galaxea 5:163–174Google Scholar
  144. Yasumoto M, Mada K, Ooi T et al (2000) New terpenoid components from the volatile oils of the soft corals Clavularia viridis and Sarcophyton acutangulum. J Nat Prod 63:1534–1536PubMedGoogle Scholar
  145. Zawada DG, Jaffe JS (2003) Changes in the fluorescence of the Caribbean coral Montastraea faveolata during heat-induced bleaching Limnol. Oceanography 48(1):412–425Google Scholar
  146. Zhang GW, Ma XQ, Kurihara H et al (2005) New hemiketal steroid from the soft coral Cladiella sp. Org Lett 7:991–994PubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of Physics and BiophysicsUniversity of SalzburgSalzburgAustria
  2. 2.Telos- Philosophische PraxisBuermoosAustria

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