Abstract
Benthic marine organisms rely on the dispersal and recruitment of propagules to replenish depleted populations following disturbances. Yet, ecological interactions between colonizing larvae and benthic competitors that become established following a disturbance can be a primary driver of recruitment success. On some coral reefs, local and global stressors have led to a proliferation of macroalgae that can inhibit the recruitment and recovery of corals. The brown macroalga Lobophora is considered a particularly strong inhibitor of coral recruitment, yet there is little information on how the alga affects demographic bottlenecks across early life-history stages. In the present study, we conducted a series of experiments to determine the effects of Lobophora sp. on three distinct life-history stages of the coral Acropora digitifera: larval settlement, early post-settlement survival, and survival and growth of small nubbins (1 cm) created from adult colonies. Our results demonstrate a high sensitivity of coral larvae to Lobophora, with settlement decreasing 16-fold when the alga was present on tiles compared to controls. Moreover, larvae did not settle on tiles when Lobophora cover > 50%. A negative, albeit minor, effect of Lobophora on the early post-settlement survival was evident, despite few recorded incidents of direct competition between settled corals and Lobophora because of low larval settlement in proximity to the alga. Conversely, there was no effect of Lobophora on the growth and survival of coral nubbins. Our results indicate that Lobophora most heavily impacts coral recruitment by inhibiting larval settlement, with the impact of the alga on recruitment decreasing through later life-history stages. These findings are concurrent with recent studies that demonstrate the ability of particular macroalgal species to deter coral larvae from settling on degraded reefs, likely through the release of chemical compounds, thereby impacting the recovery of coral populations following disturbances.
Similar content being viewed by others
References
Andras TD, Alexander TS, Gahlena A, Parry RM, Fernandez FM, Kubanek J, Wang MD, Hay ME (2012) Seaweed allelopathy against coral: surface distribution of a seaweed secondary metabolite by imaging mass spectrometry. Journal of Chemical Ecology 38:1203–1214
Arnold SN, Steneck RS, Mumby PJ (2010) Running the gauntlet: inhibitory effects of algal turfs on the processes of coral recruitment. Marine Ecology Progress Series 414:91–105
Babcock RC, Mundy CN (1996) Coral recruitment: consequences of settlement choice for early growth and survivorship in two scleractinians. Journal of Experimental Marine Biology and Ecology 206:179–201
Beatty DS, Clements CS, Stewart FJ, Hay ME (2018) Intergenerational effects of macroalgae on a reef coral: major declines in larval survival but subtle changes in microbiomes. Marine Ecology Progress Series 589:97–114
Birkeland CE (1977) The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. 1:15–21
Birrell CL, McCook LJ, Willis BL, Harrington L (2008) Chemical effects of macroalgae on larval settlement of the broadcast spawning coral Acropora millepora. Marine Ecology Progress Series 362:129–137
Box S, Mumby P (2007) Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Marine Ecology Progress Series 342:139–149
Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annual Review of Ecology and Systematics 27:477–500
Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecological Monographs 56:345–364
Chong-Seng KM, Graham NAJ, Pratchett MS (2014) Bottlenecks to coral recovery in the Seychelles. Coral Reefs 33:449–461
Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310
Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecological Monographs 67:461–488
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1:443–466
Dethier MN (1984) Disturbance and recovery in intertidal pools: maintenance of mosaic patterns. Ecological Monographs 54:99–118
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, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans RD, Williamson DH, Hoegh-Guldberg O (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS ONE 4:e5239
Dixson DL, Abrego D, Hay ME (2014) Chemically mediated behavior of recruiting corals and fishes: a tipping point that may limit reef recovery. Science 345:892–897
Doropoulos C, Roff G, Visser M-S, Mumby PJ (2017) Sensitivity of coral recruitment to subtle shifts in early community succession. Ecology 98:304–314
Doropoulos C, Roff G, Bozec Y-M, Zupan M, Werminghausen J, Mumby PJ (2016) Characterising the ecological trade-offs throughout the early ontogeny of coral recruitment. Ecological Monographs 86:20–44
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. Ecology Letters 15:338–346
Evensen NR, Doropoulos C, Morrow KM, Motti CA, Mumby PJ (2019) Inhibition of coral settlement at multiple spatial scales by a pervasive algal competitor. Marine Ecology Progress Series 612:29–42
Ferrari R, Gonzalez-Rivero M, Mumby PJ (2012) Size matters in competition between corals and macroalgae. Marine Ecology Progress Series 467:77–88
Gaines S, Roughgarden J (1985) Larval settlement rate: a leading determinant of structure in an ecological community of the marine intertidal zone. Proceedings of the National Academy of Sciences 82:3707–3711
Gosselin LA, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Marine Ecology Progress Series 146:265–282
Gouezo M, Golbuu Y, Fabricius K, Olsudong D, Mereb G, Nestor V, Wolanski E, Harrison P, Doropoulos C (2019) Drivers of recovery and reassembly of coral reef communities. Proceedings of the Royal Society B: Biological Sciences 286:20182908
Hadfield MG, Paul VJ (2001) Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae. In: McClintock J, Baker B (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 431–462
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
Harriott VJ, Fisk DA (1988) Recruitment patterns of scleractinian corals: a study of three reefs. Marine and Freshwater Research 39:409–416
Hay ME (2009) Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annual Review of Marine Science 1:193–212
Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a caribbean coral reef. Science 265:1547–1551
Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Marine Ecology Progress Series 155:269–301
Johns KA, Emslie MJ, Hoey AS, Osborne K, Jonker MJ, Cheal AJ (2018) Macroalgal feedbacks and substrate properties maintain a coral reef regime shift. Ecosphere 9:e02349
Jompa J, McCook LJ (2002) Effects of competition and herbivory on interactions between a hard coral and a brown alga. Journal of Experimental Marine Biology and Ecology 271:25–39
Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson-Williams R, Beach KS (2006) Inhibition of coral recruitment by macroalgae and cyanobacteria. Marine Ecology Progress Series 323:107–117
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82:1–26
Leong RC, Marzinelli EM, Low J, Bauman AG, Lim EWX, Lim CY, Steinberg PD, Guest JR (2018) Effect of coral-algal interactions on early life history processes in Pocillopora acuta in a highly disturbed coral reef system. Frontiers in Marine Science 5:385
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
Morrow KM, Paul VJ, Liles MR, Chadwick NE (2011) Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms. Coral Reefs 30:309–320
Morrow KM, Ritson-Williams R, Ross C, Liles MR, Paul VJ (2012) Macroalgal extracts induce bacterial assemblage shifts and sublethal tissue stress in Caribbean corals. PLoS ONE 7:e44859
Morrow KM, Bromhall K, Motti CA, Munn CB, Bourne DG (2017) Allelochemicals produced by the brown macroalga, Lobophora sp., are active against coral larvae and associated bacteria, supporting pathogenic shifts to Vibrio-dominance. Appl Environ Microbiol 83:e02391-16
Mumby PJ, Harborne AR (2010) Marine reserves enhance the recovery of corals on Caribbean reefs. PLoS ONE 5:e8657
Mumby PJ, Steneck RS, Adjeroud M, Arnold SN (2016) High resilience masks underlying sensitivity to algal phase shifts of Pacific coral reefs. Oikos 125:644–655
Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, Micheli F, Holmes KE, Dahlgren CP, Paris CB, Blackwell PG (2007) Trophic cascade facilitates coral recruitment in a marine reserve. PNAS 104:8362–8367
Nugues MM, Bak R (2006) Differential competitive abilities between Caribbean coral species and a brown alga: a year of experiments and a long-term perspective. Marine Ecology Progress Series 315:75–86
Nugues MM, Roberts CM (2003) Coral mortality and interaction with algae in relation to sedimentation. Coral Reefs 22:507–516
Paine RT, Tegner MJ, Johnson EA (1998) Compounded perturbations yield ecological surprises. Ecosystems 1:535–545
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. Marine Ecology Progress Series 426:161–170
Pineda J, Reyns NB, Starczak VR (2009) Complexity and simplification in understanding recruitment in benthic populations. Population Ecology 51:17–32
Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proceedings of the National Academy of Sciences 106:5693–5697
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proceedings of the National Academy of Sciences 107:9683–9688
Rasher DB, Stout EP, Engel S, Kubanek J, Hay ME (2011) Macroalgal terpenes function as allelopathic agents against reef corals. Proceedings of the National Academy of Sciences 108:17726–17731
Reice SR, Wissmar RC, Naiman RJ (1990) Disturbance regimes, resilience, and recovery of animal communities and habitats in lotic ecosystems. Environmental Management 14:647–659
Ritson-Williams R, Arnold SN, Paul VJ (2016) Patterns of larval settlement preferences and post-settlement survival for seven Caribbean corals. Marine Ecology Progress Series 548:127–138
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
Rodriguez SR, Ojeda FP, Inestrosa NC (1993) Settlement of benthic marine invertebrates. Marine Ecology Progress Series 97:193–207
Roff G, Doropoulos C, Zupan M, Rogers A, Steneck RS, Golbuu Y, Mumby PJ (2015) Phase shift facilitation following cyclone disturbance on coral reefs. Oecologia 178:1193–1203
Roughgarden J, Iwasa Y, Baxter C (1985) Demographic theory for an open marine population with space-limited recruitment. Ecology 66:54–67
Sammarco PW (1980) Diadema and its relationship to coral spat mortality: grazing, competition, and biological disturbance. Journal of Experimental Marine Biology and Ecology 45:245–272
Siegel DA, Mitarai S, Costello CJ, Gaines SD, Kendall BE, Warner RR, Winters KB (2008) The stochastic nature of larval connectivity among nearshore marine populations. Proceedings of the National Academy of Sciences 105:8974–8979
Skaug H, Bolker B, Magnusson A, Nielsen A (2016) Generalized Linear Mixed Models using “AD Model Builder”. R package version 0.8.3.3. http://glmmadmb.r-forge.r-project.org
Slattery M, Lesser MP (2014) Allelopathy in the tropical alga Lobophora variegata (Phaeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs? Journal of Phycology 50:493–505
Sneed JM, Sharp KH, Ritchie KB, Paul VJ (2014) The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proceedings of the Royal Society B: Biological Sciences 281:20133086
Sousa WP (1984) The role of disturbance in natural communities. Annual Review of Ecology and Systematics 15:353–391
Spencer Davies P (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Marine Biology 101:389–395
Steneck RS (1994) Is herbivore loss more damaging to reefs than hurricanes? Case studies from two Caribbean reef systems (1978–1988). In: Ginsburg RN (ed) Global aspects of coral reefs: health, hazards, and history. University of Miami Press, Miami, pp 220–225
Therneau TM (2012) coxme: Mixed effects cox models. R package version 2.2-10
Therneau TM (2015) survival: a package for survival analysis in S. R package version 2.42-6
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
Vieira C (2015) Lobophora: biotic interactions and diversification. Thesis, Ghent University
Vieira C, Thomas OP, Culioli G, Genta-Jouve G, Houlbreque F, Gaubert J, De Clerck O, Payri CE (2016) Allelopathic interactions between the brown algal genus Lobophora (Dictyotales, Phaeophyceae) and scleractinian corals. Scientific Reports 6:18637
Webster NS, Smith LD, Heyward AJ, Watts JEM, Webb RI, Blackall LL, Negri AP (2004) Metamorphosis of a scleractinian coral in response to microbial biofilms. Applied and Environmental Microbiology 70:1213–1221
Acknowledgements
We thank L. Puk, F. Peiffer, C. Wiseman, A. Kavanagh, J. Smart, M. Dyring, and M. Naugle who assisted with field work in Palau. We also thank the staff from the Palau International Coral Reef Center for hosting us during our trip to Palau. Two anonymous reviewers and Raphael Ritson-Williams provided valuable feedback that substantially improved the manuscript. This work was funded by ARC grants awarded to PJM.
Author information
Authors and Affiliations
Corresponding author
Additional information
Topic Editor Morgan S. Pratchett
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Evensen, N.R., Doropoulos, C., Wong, K.J. et al. Stage-specific effects of Lobophora on the recruitment success of a reef-building coral. Coral Reefs 38, 489–498 (2019). https://doi.org/10.1007/s00338-019-01804-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-019-01804-w