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Alternate coral–bryozoan competitive superiority during coral bleaching

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Abstract

Bleaching of corals results from the loss of their symbiotic algae (zooxanthellae) and/or pigments. The supply of photoassimilates provided by the zooxanthellae to the coral declines during bleaching and reduces the ability to activate energy-costly processes such as maintenance, growth and reproduction. In the present study we compared the competitive outcomes, expressed as overgrowth and changes in colony sizes of Oculina patagonica (an encrusting Mediterranean stony coral) and the bryozoan Watersipora sp., growing in contact with each other, during and between bleaching events. Year-round observations of tagged colonies showed alternating competitive outcomes: O. patagonica wins over Watersipora sp. between bleaching events, but loses during bleaching events. Using the 14C-point-labeling technique on coral tissue, we examined intra-colonial translocation of photosynthetic products from the point-tissue labeling towards interaction zones. In non-bleached O. patagonica, competition resulted in preferentially oriented translocation of 14C products to the interaction zone located up to 8 cm away from the tissue-labeling site. Sites opposite the interaction zone received significantly less labeled photoassimilates compared to the interaction zone. In bleached colonies (40–85% bleached surface area), such translocation did not occur, probably explaining the failure to compete with the encrusting neighbor Watersipora sp. Our findings demonstrate the importance of colonial integration and resource orientation for the competitive superiority of O. patagonica.

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References

  • Alino PM, Sammarco PW, Coll JC (1992) Competitive strategies in soft corals (Coelenterata, Octocorallia). 4. Environmentally induced reversals in competitive superiority. Mar Ecol Prog Ser 81:129–145

    Google Scholar 

  • Bak RPM (1983) Neoplasia regeneration and growth in the reef building coral Acropora palmata. Mar Biol 77:221–227

    Google Scholar 

  • Bak RPM, Steward-Van Es Y (1980) Regeneration of superficial damage in the scleractinian corals Agaricia agarites, Favia purpuvea and Porites astroides. Bull Mar Sci 30:883–887

    Google Scholar 

  • Barnes DKA, Rothery P (1996) Competition in encrusting Antarctic bryozoan assemblages: outcomes influences and implications. J Exp Mar Biol Ecol 196:267–284

    Article  Google Scholar 

  • Brown BE, Suharsono (1990) Damage and recovery of coral reefs affected by El Niño related seawater warming in the Thousand Islands, Indonesia. Coral Reefs 8:163–170

    Google Scholar 

  • Brown BH (1997) Coral bleaching: causes and consequences. In: Lessios HA, MacIntyre IG (eds) Proc 8th Int Coral Reef Symp. Smithsonian Tropical Research Institute, Balboa, Panama, pp 65–74

  • Buss LW (1980) Bryozoan overgrowth interactions—the interdependence of competition for space and food. Nature 281:475–477

    Google Scholar 

  • Buss LW, Jackson JBC (1979) Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am Nat 113:223–234

    Article  Google Scholar 

  • Chornesky EA (1989) Repeated reversals during spatial competition between corals. Ecology 70:843–855

    Google Scholar 

  • Connell JH (1961) The influence of interspecific competition and other factors on the distribution of the barnacle Chtamalus stellatus. Ecology 42:710–723

    Google Scholar 

  • Crossland CJ, Barnes DJ, Cox T, Devereux M (1980) Compartmentation and turnover of organic carbon in the staghorn coral Acropora formosa. Mar Biol 59:181–187

    CAS  Google Scholar 

  • Dayton PK (1971) Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389

    Google Scholar 

  • Done TJ (1999) Coral community adaptability to environmental change at the scales of regions, reefs and reef zones. Am Zool 39:66–79

    Google Scholar 

  • Fine M, Zibrowius H, Loya Y (2001) Oculina patagonica: A non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar Biol 138:1195–1203

    Article  Google Scholar 

  • Fine M, Oren U, Loya Y (2002) Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica. Mar Ecol Prog Ser 234:119–125

    Google Scholar 

  • Gattuso JP, Yellowlees D, Lesser M (1993) Depth- and light-dependent variation of carbon partitioning and utilization in the zooxanthellate scleractinian coral Stylophora pistillata. Mar Ecol Prog Ser 92:267–276

    Google Scholar 

  • Gleason MG (1993) Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia. Coral Reefs 12:193–201

    Google Scholar 

  • Glynn PW (1988) El Niño–Southern Oscillation 1982–1983: near shore population, community, and ecosystem responses. Annu Rev Ecol Syst 19:309–345

    Article  Google Scholar 

  • Glynn PW (1993) Coral-reef bleaching—ecological perspectives. Coral Reefs 12:1–17

    Google Scholar 

  • Goreau TJ, Macfarlane AH (1990) Reduced growth rate of Montastrea annularis following the 1987–1988 coral-bleaching event. Coral Reefs 8:211–215

    Google Scholar 

  • Guzman MG, Cortes J (2001) Changes in reef community structure after fifteen years of natural disturbances in the eastern pacific (Costa Rica). Bull Mar Sci 69:133–149

    Google Scholar 

  • Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinski Z (ed) Coral reefs. Ecosystems of the world 25. Elsevier, Amsterdam, pp 133–206

  • Harvell CD (1990) Density effects in a colonial monoculture: experimental studies with a marine bryozoan (Membraneopora membranacea L). Oecologia 82:227–237

    Google Scholar 

  • Harvell CD (1998) Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52:80–86

    Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change coral bleaching and the world's coral reefs. Mar Freshwater Res 50:839–866

    Google Scholar 

  • Kellogg RB, Patton JS (1983) Lipid droplets, medium of energy exchange in the symbiotic anemone, Condylactis gigantea: a model coral polyp. Mar Biol 75:137–149

    CAS  Google Scholar 

  • Koh EGL, Sweatman H (2000) Chemical warfare among scleractinians: bioactive natural products from Tubastrea faulkneri Wells krill larvae of potential competitors. J Exp Mar Biol Ecol 251:141–160

    Article  CAS  PubMed  Google Scholar 

  • Kozlowski J, Wiegert RG (1986) Optimal allocation of energy to growth and reproduction. Theor Popul Biol 29:16–37

    CAS  PubMed  Google Scholar 

  • Kushmaro A, Loya Y, Fine M, Rosenberg E (1996) Bacterial infection and bleaching. Nature 380:396

    CAS  Google Scholar 

  • Kushmaro A, Rosenberg E, Fine M, Loya Y (1998) Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar Ecol Prog Ser 171:131–137

    Google Scholar 

  • Lang JC, Chornesky EA (1990) Competition between scleractinian reef corals—a review of mechanisms and effects. In: Dubinski Z (ed) Coral reefs. Ecosystems of the world 25. Elsevier, Amsterdam, pp 133–206

  • Loya Y (1976) The Red Sea coral Stylophora pistillata is an r strategist. Nature 259:478–480

    Google Scholar 

  • Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131

    Article  Google Scholar 

  • Meesters EH, Bak RPM (1993) Effects of coral bleaching on tissue regeneration potential and colony survival. Mar Ecol Prog Ser 96:189–198

    Google Scholar 

  • Miles JS, Harvell CD, Griggs CM, Eisner S (1995) Resource translocation in a marine bryozoan: quantification and visualization of 14C and 35S. Mar Biol 122:439–445

    Google Scholar 

  • Muscatine L (1973) Nutrition of corals. In: Jones OA, Endean R (eds) Biology and geology of coral reefs, vol 2. Academic, New York

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reefs 25:1–29

    Google Scholar 

  • Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull (Woods Hole) 137:506–523

    Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: naturalistic symbiosis adapted to nutrient poor environments. BioScience 27:454–460

    Google Scholar 

  • Muscatine L, McCloskey LR, Marian RF (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    CAS  Google Scholar 

  • Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of photosynthetically fixed carbon and light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B Biol Sci 222:181–202

    CAS  Google Scholar 

  • Nandakumar K, Tanaka M, Kikuchi T (1993) Interspecific competition among fouling organisms in Tomioka Bay, Japan. Mar Ecol Prog Ser 94:43–50

    Google Scholar 

  • Oren U, Rinkevich B, Loya Y (1997) Oriented intra-colonial transport of 14C labeled materials during regeneration in scleractinian corals. Mar Ecol Prog Ser 161:117–121

    Google Scholar 

  • Oren U, Brickner I, Loya Y (1998) Prudent sessile feeding by the corallivore snail Coralliophila violacea on coral energy sinks. Proc R Soc Lond B Biol Sci 265:2043–2050

    Article  Google Scholar 

  • Oren U, Benayahu Y, Lubinevsky H, Loya Y (2001) Extent of coral colony integration during regeneration. Ecology 82:802–813

    Google Scholar 

  • Pearse VB, Muscatine L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Biol Bull (Woods Hole) 141:350–363

    Google Scholar 

  • Peres JM (1967) The Mediterranean benthos. Oceanogr Mar Biol Annu Rev 5:449–533

    Google Scholar 

  • Porter JM (1974) Community structure of coral reefs on opposite sides of the Isthmus of Panama. Science 186:543–545

    Google Scholar 

  • Rinkevich B (1989) The contribution of photosynthetic products to coral reproduction. Mar Biol 101:259–263

    CAS  Google Scholar 

  • Rinkevich B, Loya Y (1984) Coral illumination through an optic-fiber: incorporation of 14C photosynthates. Mar Biol 80:7–15

    CAS  Google Scholar 

  • Romano SL (1990) Long-term effects of interspecific aggression on growth of the reef building corals Cyphastrea ocellina (Dana) and Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 140:135–146

    Google Scholar 

  • Sara M, Vacelet J (1973) Ecologie des demosonges. In: Traite de zoologie, tome 3, fasc. 1. Spongiaires. Masson et Ce, Liberaire de l'Academie de Medicine, Paris, pp 462–576

  • Sebens KP (1986) Spatial relationships among encrusting marine organisms in the New England subtidal zone. Ecol Monogr 56:73–96

    Google Scholar 

  • Stebbing ARD (1973) Observations on colony overgrowth and spatial competition. In: Larwood GP (ed) Living and fossil Bryozoa. Academic, London, pp 173–183

  • Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904

    Google Scholar 

  • Sullivan B, Faulkner DJ, Webb L (1983) Siphonodictidine, a metabolite of the burrowing sponge Siphonodictyon sp. that inhibits coral growth. Science 221:1175–1176

    CAS  Google Scholar 

  • Swanson R, Hoegh-Guldberg O (1998) The assimilation of ammonium by the symbiotic sea anemone Aiptasia pulchella. Mar Biol 131:83–93

    CAS  Google Scholar 

  • Szmant-Froelich AM (1985) The effect of colony size on the reproductive ability of the Caribbean coral Montastrea annularis (Ellis and Solander). In: Gabrié C, et al (eds) Proc 5th Int Coral Reef Congr, vol 4. Antenne Museum—EPHE, Moorea, French Polynesia, pp 295–300

  • Taylor DL (1977) Intra-colonial transport of organic compounds and calcium in some Atlantic reef corals. In: Taylor DL (ed) Proc 3rd Int Coral Reef Symp. University of Miami, Miami, pp 431–436

  • Trench RK (1979) The cell biology of plant–animal symbiosis. Annu Rev Plant Physiol 30:485–531

    CAS  Google Scholar 

  • Turner SJ, Todd CD (1994) Competition for space in encrusting bryozoan assemblages: the influence of encounter angle, site and year. J Mar Biol Assoc UK 74:603–622

    Google Scholar 

  • Underwood AJ (1979) The ecology of intertidal gastropods. Adv Mar Biol 16:111–210

    Google Scholar 

  • Underwood AJ (1992) Competition and marine plant–animal interactions. In: John DM, Hawkins SJ, Price JH (eds) Plant–animal interactions in the marine benthos. Systematic Association special volume 46, Clarendon, Oxford, pp 443–475

  • van Woesik R (2002) Processes regulating coral communities. Commun Theor Biol 7:199–212

    Google Scholar 

  • Wilkinson CR (2000) The 1997–98 mass coral bleaching and mortality event: 2 years on. In: Wilkinson CR (ed) Status of coral reefs of the world: 2000. Australian Institute of Marine Science, Townsville, pp 21–35

    Google Scholar 

  • Zibrowius H, Ramos A (1983) Oculina patagonica, scleractiniare exotique en Mediterranee—nouvelles observations dans le sud-est de l'Espagne. Rapp P-V Reun Comm Int Explor Sci Mer Mediterr 28:297–301

    Google Scholar 

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Acknowledgements

We are grateful to N. Paz for her editorial assistance and to O. Mokady for valuable remarks on an earlier version of this manuscript. This research was supported by the Raynor Chair for Environmental Conservation Research to Y.L. and the Rieger Fellowship to M.F. All sampling and experiments carried out during this study comply with the laws for protection of nature of the State of Israel and were carried out under special permits from the Nature Reserve Authorities.

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Correspondence to Y. Loya.

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Communicated by O. Kinne, Oldendorf/Luhe

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Fine, M., Loya, Y. Alternate coral–bryozoan competitive superiority during coral bleaching. Marine Biology 142, 989–996 (2003). https://doi.org/10.1007/s00227-002-0982-7

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