Abstract
The resilience of coral reefs relies significantly on the ability of corals to recover successfully in algal-dominated environments. Larval settlement is a critical but highly vulnerable stage in the early life history of corals. In this study, we analyzed how the presence of two upright fleshy algae, Sargassum mcclurei (SM) and Padina australis (PA), and one crustose coralline algae, Mesophyllum simulans (MS), affects the settlement of Acropora muricata larvae. Coral larvae were exposed to seawater flowing over these algae at two concentrations. Larval settlement and mortality were assessed daily through four variables related to their behavior: swimming, substratum testing, metamorphosis, and stresses. Temperature, dissolved oxygen, pH, algal growth, and photosynthetic efficiency were monitored throughout the experiment. Results showed that A. muricata larvae can settle successfully in the absence of external stimuli (63 ± 6 % of the larvae settled in control treatments). While algae such as MS may stimulate substrate testing and settlement of larvae in the first day after competency, they ultimately had a lower settlement rate than controls. Fleshy algae such as PA, and in a lesser measure SM, induced more metamorphosis than controls and seemed to eventually stimulate settlement. A diverse combination of signals and/or modifications of microenvironments by algae and their associated microbial communities may explain the pattern observed in coral settlement. Overall, this study contributes significantly to the knowledge of the interaction between coral and algae, which is critical for the resilience of the reefs.
References
Abelson A, Denny M (1997) Settlement of marine organisms in flow. Annu Rev Ecol Syst 28:317–339
Amsler CD, Reed DC, Neushul M (1992) The microclimate inhabited by macroalgal propagules. Br Phycol J 27:253–270
Anthony KRN, Kleypas JA, Gattuso JP (2011) Coral reefs modify their seawater carbon chemistry – implications for impacts of ocean acidification. Global Change Biol 17:3655–3666
Arnold SN, Steneck RS, Mumby PJ (2010) Running the gauntlet: inhibitory effects of algal turfs on the processes of coral recruitment. Mar Ecol Prog Ser 414:91–105
Axelsson L, Ryberg H, Beer S (1995) Two modes of bicarbonate utilization in the marine green macroalga Ulva lactuca. Plant Cell Environ 18:439–445
Baird AH, Babcock RC, Mundy CP (2003) Habitat selection by larvae influences the depth distribution of six common coral species. Mar Ecol Prog Ser 252:289–293
Barnes DJ (1983) Profiling coral reef productivity and calcification using pH and oxygen electrodes. J Exp Mar Biol Ecol 66:149–161
Barnes DJ, Lazar B (1993) Metabolic performance of a shallow reef patch near Eilat on the Red sea. J Exp Mar Biol Ecol 174:1–13
Barott KL, Rodriguez-Mueller B, Youle M, Marhaver KL, Vermeij MJA, Smith JE, Rohwer FL (2012) Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae. Proc R Soc Lond B Biol Sci 279:1655–1664
Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes? Global Change Biol 19:2613–2624
Birkeland C (1977) The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. Proc 3rd Int Coral Reef Symp 1:15–22
Birrell CL, McCook LJ, Willis BL, Diaz-Pulido GA (2008a) Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanogr Mar Biol Annu Rev 46:25–64
Birrell CL, McCook LJ, Willis BL, Harrington L (2008b) Chemical effects of macroalgae on larval settlement of the broadcast spawning coral Acropora millepora. Mar Ecol Prog Ser 362:129–137
Chen CA, Dai C-F (2004) Local phase shift from Acropora-dominant to Condylactis-dominant community in the Tiao-Shi Reef, Kenting National Park, southern Taiwan. Coral Reefs 23:508
Diaz-Pulido G, McCook LJ (2002) The fate of bleached corals: patterns and dynamics of algal recruitment. Mar Ecol Prog Ser 232:115–128
Diaz-Pulido G, Harii S, McCook LJ, Hoegh-Guldberg O (2010) The impact of benthic algae on the settlement of a reef-building coral. Coral Reefs 29:203–208
Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony K (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162
Doropoulos C, Diaz-Pulido G (2013) High CO2 reduces the settlement of a spawning coral on three common species of crustose coralline algae. Mar Ecol Prog Ser 475:93–99
Doropoulos C, Ward S, Diaz-Pulido G, Hoegh-Guldberg O, Mumby PJ (2012) Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol Lett 15:338–346
Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annual Review of Ecology, Evolution, and Systematics 35:557–581
Fox J, Weisberg S (2010) An R companion to applied regression. Sage, California
Frankignoulle M, Gattuso JP, Biondo R, Bourge I, CopinMontegut G, Pichon M (1996) Carbon fluxes in coral reefs II: Eulerian study of inorganic carbon dynamics and measurements of air-sea CO2 exchanges. Mar Ecol Prog Ser 145:123–132
Gattuso JP, Pichon M, Delesalle B, Canon C, Frankignoulle M (1996) Carbon fluxes in coral reefs I: Lagrangian measurement of community metabolism and resulting air-sea CO2 disequilibrium. Mar Ecol Prog Ser 145:109–121
Gleason DF, Hofmann DK (2011) Coral larvae: from gametes to recruits. J Exp Mar Biol Ecol 408:42–57
Gleason DF, Danilowicz BS, Nolan CJ (2009) Reef waters stimulate substratum exploration in planulae from brooding Caribbean corals. Coral Reefs 28:549–554
Gribben PE, Marshall DJ, Steinberg PD (2006) Less inhibited with age? Larval age modifies responses to natural settlement inhibitors. Biofouling 22:101–106
Hadfield MG, Paul VJ (2001) Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae. In: McClintock JB, Baker W (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 431–461
Harrington L, Fabricius K, De’Ath G, Negri A (2004) Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428–3437
Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. Ecosyst World 25:133–207
Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145
Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551
Hughes TP, Bellwood DR, Folke C, Steneck RS, Wilson J (2005) New paradigms for supporting the resilience of marine ecosystems. Trends Ecol Evol 20:380–386
Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365
ICRS (2012) Support the consensus statement on climate change and coral reefs. http://www.icrs2012.com/Consensus_Statement.htm (accessed 01.08.2013)
Johnson CR, Sutton DC (1994) Bacteria on the surface of crustose coralline algae induce metamorphosis of the crown-of-thorns starfish Acanthaster planci. Mar Biol 120:305–310
Kerswell AP (2006) Global biodiversity patterns of benthic marine algae. Ecology 87:2479–2488
Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson-Williams R, Beach KS (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323:107–111
Maypa AP, Raymundo LJ (2004) Algae-coral interactions: mediation of coral settlement, early survival and growth by macroalgae. Silliman Journal 45:76–95
McCook L, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417
Morse DE, Hooker N, Morse AN, Jensen RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Biol Ecol 116:193–217
Mumby PJ (2009a) Phase shifts and the stability of macroalgal communities on Caribbean. Coral Reefs 28:761–773
Mumby PJ (2009b) Herbivory versus corallivory: are parrotfish good or bad for Caribbean coral reefs? Coral Reefs 28:683–690
Negri AP, Webster NS, Hill RT, Heyward AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser 223:121–131
Niggel W, Haas AF, Wild C (2010) Benthic community composition affects O2 availability and variability in a Northern Red Sea fringing reef. Hydrobiologia 644:401–405
Nugues MM, Szmant AM (2006) Coral settlement onto Halimeda opuntia: a fatal attraction to an ephemeral substrate? Coral Reefs 25:585–591
Paul VJ, Kuffner IB, Walters LJ, Ritson-Williams R, Beach KS, Becerro MA (2011) Chemically mediated interactions between macroalgae Dictyota spp. and multiple life-history stages of the coral Porites astreoides. Mar Ecol Prog Ser 426:161–170
Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Annu Rev 30:273–335
Raimondi PT, Morse AN (2000) The consequences of complex larval behavior in a coral. Ecology 81:3193–3211
Ritson-Williams R, Paul VJ, Arnold SN, Steneck RS (2010) Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis. Coral Reefs 29:71–81
Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij MJ, Paul VJ (2009) New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson Contrib Mar Sci 38:437–457
Rodriguez SR, Ojeda FP, Inestrosa NC (1993) Settlement of benthic marine invertebrates. Mar Ecol Prog Ser 97:193–207
Semesi IS, Beer S, Björk M (2009) Seagrass photosynthesis controls rates of calcification and photosynthesis of calcareous macroalgae in a tropical seagrass meadow. Mar Ecol Prog Ser 382:41–47
Shamberger KEF, Feely RA, Sabine CL, Atkinson MJ, DeCarlo EH, Mackenzie FT, Drupp PS, Butterfield DA (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75
Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461
Shearer TL, Rasher DB, Snell TW, Hay ME (2012) Gene expression patterns of the coral Acropora millepora in response to contact with macroalgae. Coral Reefs 31:1177–1192
Smith JE, Price NN, Nelson CE, Haas AF (2013) Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms. Mar Biol 160:2437–2447
Steneck RS, Paris CB, Arnold SN, Ablan-Lagman MC, Alcala AC, Butler MJ, McCook LJ, Russ GR, Sale PF (2009) Thinking and managing outside the box: coalescing connectivity networks to build region-wide resilience in coral reef ecosystems. Coral Reefs 28:367–378
Stevens JP (2002) Applied multivariate statistics for the social sciences, 4th edn. Lawrence Erlbaum Association, Mahwah, NJ
Tran C, Hadfield MG (2011) Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Mar Ecol Prog Ser 433:85–96
Venera-Ponton DE, Diaz-Pulido G, McCook LJ, Rangel-Campo A (2011) Macroalgae reduce growth of juvenile corals but protect them from parrotfish damage. Mar Ecol Prog Ser 421:109–115
Vermeij MJA (2006) Early life-history dynamics of Caribbean coral species on artificial substratum: the importance of competition, growth and variation in life-history strategy. Coral Reefs 25:59–71
Vermeij MJ (2009) Floating corallites: a new ecophenotype in scleractinian corals. Coral Reefs 28:987
Walters LJ, Hadfield MG, Smith CM (1996) Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement. Mar Biol 126:383–393
Walters LJ, Smith CM, Hadfield MG (2003) Recruitment of sessile marine invertebrates on Hawaiian macrophytes: do pre-settlement or post-settlement processes keep plants free from fouling? Bull Mar Sci 72:813–839
Webster NS, Soo R, Cobb R, Negri AP (2010) Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae. ISME J 5:759–770
Webster NS, Smith LD, Heyward AJ, Watts JE, Webb RI, Blackall LL, Negri AP (2004) Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl Environ Microbiol 70:1213–1221
Whalan S, Webster NS, Negri AP (2012) Crustose coralline algae and a cnidarian neuropeptide trigger larval settlement in two coral reef sponges. PLoS ONE 7:e30386 [doi:10.1371/journal.pone.0030386]
Wild C, Niggel W, Naumann MS, Haas AF (2010) Organic matter release by Red Sea coral reef organisms – potential effects on microbial activity and in situ O2 availability. Mar Ecol Prog Ser 411:61–71
Work TM, Aeby GS, Maragos JE (2008) Phase shift from a coral to a corallimorph-dominated reef associated with a shipwreck on Palmyra Atoll. PLoS ONE 3:e2989 [doi:10.1371/journal.pone.0002989]
Zeebe RE, Wolf-Gladrow DA, Jansen H (1999) On the time required to establish chemical and isotopic equilibrium in the carbon dioxide system in seawater. Mar Chem 65:135–153
Acknowledgements
We are grateful to the staff of the Penghu Marine Biological Research Center and members of the Coral Lab for helping us to perform this experiment. We also thank Dr. Yoko Nozawa and Julia Ka Lai Leung for their useful comments and advice on this manuscript and Michael Honeth for English editing. This work was supported by a grant from Academia Sinica (AS-100-TP2-A02-3). VD is the recipient of a postdoctoral fellowship from the National Science Council of Taiwan, ML and SSD of a grant from the Taiwan International Graduate Program, and SK by a postdoctoral fellowship from Academia Sinica. This is a contribution #88 of Coral Lab, Biodiversity Research Center, Academia Sinica.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Mark Vermeij
V. Denis and M. Loubeyres have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
338_2014_1127_MOESM1_ESM.eps
Supplementary material Figure S1. Light conditions around experimental tanks. Gray numbers indicate irradiance (μmol photons m-2) measured using a quantum sensor (LI193SA, LICOR) on two sides of the tanks. Difference among treatments was tested using a nonparametric Kruskal–Wallis test. CO: control, PA: Padina australis, SM: Sargassum mcclurei, MS: Mesophyllum simulans. 1 and 4 represent 1 g and 4 g treatments, respectively (EPS 982 kb)
Rights and permissions
About this article
Cite this article
Denis, V., Loubeyres, M., Doo, S.S. et al. Can benthic algae mediate larval behavior and settlement of the coral Acropora muricata? . Coral Reefs 33, 431–440 (2014). https://doi.org/10.1007/s00338-014-1127-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-014-1127-4