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Interannual variability and decadal stability of benthic organisms on an Indonesian coral reef

Published online by Cambridge University Press:  03 May 2021

Alberto Rovellini Open the ORCID record for Alberto Rovellini [Opens in a new window] ,
Matthew R. Dunn ,
Elizabeth A. Fulton ,
Lisa Woods ,
Jamaluddin Jompa ,
Abdul Haris  and
James J. Bell Open the ORCID record for James J. Bell [Opens in a new window]
Alberto Rovellini*
Affiliation:
School of Biological Sciences, Victoria University of Wellington, Wellington6012, New Zealand
Matthew R. Dunn
Affiliation:
National Institute of Water and Atmospheric Research (NIWA), Wellington6021, New Zealand
Elizabeth A. Fulton
Affiliation:
CSIRO Oceans and Atmosphere, Hobart7004Tasmania, Australia Centre for Marine Socioecology, University of Tasmania, Hobart, Australia
Lisa Woods
Affiliation:
School of Mathematics and Statistics, Victoria University of Wellington, Wellington6012, New Zealand
Jamaluddin Jompa
Affiliation:
Department of Marine Science, Universitas Hasanuddin, Makassar90245, Indonesia
Abdul Haris
Affiliation:
Department of Marine Science, Universitas Hasanuddin, Makassar90245, Indonesia
James J. Bell
Affiliation:
School of Biological Sciences, Victoria University of Wellington, Wellington6012, New Zealand
*
Author for correspondence: Alberto Rovellini, Email: [email protected]
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Abstract

The availability of colonizable substrate is an important driver of the temporal dynamics of sessile invertebrates on coral reefs. Increased dominance of algae and, in some cases, sponges has been documented on many coral reefs around the world, but how these organisms benefit from non-colonized substrate on the reef is unclear. In this study, we described the temporal dynamics of benthic organisms on an Indonesian coral reef across two time periods between 2006 and 2017 (2006–2008 and 2014–2017), and investigated the effects of colonizable substrate on benthic cover of coral reef organisms at subsequent sampling events. In contrast with other Indonesian reefs where corals have been declining, corals were dominant and stable over time at this location (mean ± SE percentage cover 42.7 ± 1.9%). Percentage cover of turf algae and sponges showed larger interannual variability than corals and crustose coralline algae (CCA) (P < 0.001), indicating that these groups are more dynamic over short temporal scales. Bare substrate was a good predictor of turf cover in the following year (mean effect 0.2, 95% CI: 0–0.4). Algal cover combined with bare space was a good predictor of CCA cover the following year generally, and of sponge cover the following year but only at one of the three sites. These results indicate that turf algae on some Indonesian reefs can rapidly occupy free space when this becomes available, and that other benthic groups are probably not limited by the availability of bare substrate, but may overgrow already fouled substrates.

Keywords

Bare substratebenthic dynamicsdecadal stabilityIndonesian coral reefsinterannual variability
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 2 , March 2021 , pp. 221 - 231
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Adjeroud, M, Augustin, D, Galzin, R and Salvat, B (2002) Natural disturbances and interannual variability of coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997. Marine Ecology Progress Series 237, 121–131.CrossRefGoogle Scholar
Adjeroud, M, Poisson, E, Peignon, C, Penin, L and Kayal, M (2019) Spatial patterns and short-term changes of coral assemblages along a cross-shelf gradient in the southwestern lagoon of New Caledonia. Diversity 11, 21.CrossRefGoogle Scholar
Anderson, MJ (2001) A new method for non parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Anderson, MJ and Willis, TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84, 511–525.CrossRefGoogle Scholar
Arnold, SN and Steneck, RS (2011) Settling into an increasingly hostile world: the rapidly closing ‘recruitment window’ for corals. PLoS ONE 6, e28681.CrossRefGoogle Scholar
Bailey-Brock, JH (1989) Fouling community development on an artificial reef in Hawaiian waters. Bulletin of Marine Science 44, 580–591.Google Scholar
Bell, JJ and Smith, D (2004) Ecology of sponge assemblages (Porifera) in the Wakatobi region, south-east Sulawesi, Indonesia: richness and abundance. Journal of the Marine Biological Association of the United Kingdom 84, 581–591.CrossRefGoogle Scholar
Bell, JJ, Biggerstaff, A, Bates, T, Bennett, H, Marlow, J, McGrath, E and Shaffer, M (2017) Sponge monitoring: moving beyond diversity and abundance measures. Ecological Indicators 78, 470–488.CrossRefGoogle Scholar
Bell, JJ, Jompa, J, Haris, A, Werorilangi, S, Shaffer, M and Mortimer, C (2018) Domination of mesophotic ecosystems in the Wakatobi Marine National Park (Indonesia) by sponges, soft corals and other non-hard coral species. Journal of the Marine Biological Association of the United Kingdom 99, 771–775.CrossRefGoogle Scholar
Biggerstaff, A, Jompa, J and Bell, JJ (2017) Increasing benthic dominance of the phototrophic sponge Lamellodysidea herbacea on a sedimented reef within the Coral Triangle. Marine Biology 164, 1–16.CrossRefGoogle Scholar
Boschetti, ST (2016) Impact of the local environmental variability on the patterns of coral recruitment on Indo-Pacific reefs (PhD thesis). Victoria University of Wellington, New Zealand.Google Scholar
Brown, BE and 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.CrossRefGoogle Scholar
Bruno, JF and Selig, ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 2, e711.CrossRefGoogle ScholarPubMed
Bruno, JF, Sweatman, H, Precht, WF, Selig, ER and Schutte, VGW (2009) Assessing evidence of phase shifts to macroalgal dominance on coral reefs. Ecology 90, 1478–1484.CrossRefGoogle ScholarPubMed
Carballo, JL (2006) Effect of natural sedimentation on the structure of tropical rocky sponge assemblages. Ecoscience 13, 119–130.CrossRefGoogle Scholar
Cheshire, AC and Wilkinson, CR (1991) Modelling the photosynthetic production by sponges on Davies Reef, Great Barrier Reef. Marine Biology 18, 13–18.CrossRefGoogle Scholar
Clifton, J and Unsworth, RK (2010) Introduction. In Clifton, J, Unsworth, R and Smith, DJ (eds), Marine Research and Conservation in the Coral Triangle: The Wakatobi Marine National Park. New York, NY: Nova Publishers, pp. 1–9.Google Scholar
Clifton, J, Unsworth, RRK and Smith, DJ (2010) Marine Research and Conservation in the Coral Triangle. The Wakatobi National Park. New York, NY: Nova Publishers.Google Scholar
Cooper, JK, Spencer, M and Bruno, JF (2015) Stochastic dynamics of a warmer Great Barrier Reef. Ecology 96, 1802–1811.CrossRefGoogle ScholarPubMed
Crabbe, MJC and Smith, DJ (2005) Sediment impacts on growth rates of Acropora and Porites corals from fringing reefs of Sulawesi, Indonesia. Coral Reefs 24, 437–441.CrossRefGoogle Scholar
Crisp, DJ and Ryland, JS (1960) Influence of filming and of surface texture on the settlement of marine organisms. Nature 185, 119.CrossRefGoogle Scholar
Dinesen, Z (1983) Shade-dwelling corals of the Great Barrier Reef. Marine Ecology Progress Series 10, 173–185.CrossRefGoogle Scholar
Dinno, A (2017) dunn.test: Dunn's Test of multiple comparisons using rank sums. R package version 1.3.5. Available at: https://cran.r-project.org/package=dunn.test.Google Scholar
Draisma, SGA, Prud'homme van Reine, WF, Herandarudewi, SMC and Hoeksema, BW (2018) Macroalgal diversity along an inshore-offshore environmental gradient in the Jakarta Bay Thousand Islands reef complex, Indonesia. Estuarine, Coastal and Shelf Science 200, 258–269.CrossRefGoogle Scholar
Edinger, EN, Jompa, J, Limmon G, V., Widjatmoko, W and Risk, MJ (1998) Reef degradation and coral biodiversity in Indonesia: effects of land-based pollution, destructive fishing practices and changes over time. Marine Pollution Bulletin 36, 617–630.CrossRefGoogle Scholar
Fang, JKH, Mason, RAB, Schönberg, CHL, Hoegh-Guldberg, O and Dove, S (2017) Studying interactions between excavating sponges and massive corals by the use of hybrid cores. Marine Ecology 38, e12393.CrossRefGoogle Scholar
González-Rivero, M, Yakob, L and Mumby, PJ (2011) The role of sponge competition on coral reef alternative steady states. Ecological Modelling 222, 1847–1853.CrossRefGoogle Scholar
González-Rivero, M, Ferrari, R, Schönberg, CHL and Mumby, PJ (2012) Impacts of macroalgal competition and parrotfish predation on the growth of a common bioeroding sponge. Marine Ecology Progress Series 444, 133–142.CrossRefGoogle Scholar
González-Rivero, M, Bozec, YM, Chollett, I, Ferrari, R, Schönberg, CHL and Mumby, PJ (2016) Asymmetric competition prevents the outbreak of an opportunistic species after coral reef degradation. Oecologia 181, 161–173.CrossRefGoogle ScholarPubMed
Gouraguine, A, Moranta, J, Ruiz-Frau, A, Hinz, H, Reñones, O, Ferse, SCA, Jompa, J and Smith, DJ (2019) Citizen science in data and resource-limited areas: a tool to detect long-term ecosystem changes. PLoS ONE 14, e0210007.CrossRefGoogle ScholarPubMed
Gross, K, Edmunds, PJ and Holmes, EE (2015) Stability of Caribbean coral communities quantified by long-term monitoring and autoregression models. Ecology 96, 1812–1822.CrossRefGoogle ScholarPubMed
Heron, SF, Maynard, JA, Van Hooidonk, R and Eakin, CM (2016) Warming trends and bleaching stress of the world's coral reefs 1985–2012. Scientific Reports 6, 38402.CrossRefGoogle ScholarPubMed
Heyward, AJ and Negri, AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18, 273–279.CrossRefGoogle Scholar
Hoeksema, BW (1991) Control of bleaching in mushroom coral populations (Scleractinia: Fungiidae) in the Java Sea: stress tolerance and interference by life history strategy. Marine Ecology Progress Series 74, 225–237.CrossRefGoogle Scholar
Hoeksema, BW (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. Biogeography, Time, and Place: Distributions, Barriers, and Islands 29, 117–178.Google Scholar
Hughes, TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551.CrossRefGoogle ScholarPubMed
Hughes, TP, Kerry, JT, Álvarez-Noriega, M, Álvarez-Romero, JG, Anderson, KD, Baird, AH, Babcock, RC, Beger, M, Bellwood, DR, Berkelmans, R, Bridge, T, Butler, IR, Byrne, M, Cantin, NE, Comeau, S, Connolly, SR, Cumming, GS, Dalton, SJ, Diaz-Pulido, G, Eakin, CM, Figueira, WF, Gilmour, JP, Harrison, HB, Heron, SF, Hoey, AS, Hobbs, J-PA, Hoogenboom, MO, Kennedy, EV, Kuo, C-y, Lough, JM, Lowe, RJ, Liu, G, McCulloch, MT, Malcolm, HA, McWilliam, MJ, Pandolfi, JM, Pears, RJ, Pratchett, MS, Schoepf, V, Simpson, T, Skirving, WJ, Sommer, B, Torda, G, Wachenfeld, DR, Willis, BL and Wilson, SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543, 373–378.CrossRefGoogle ScholarPubMed
Knapp, ISS, Williams, GJ, Carballo, JL, Cruz-Barraza, JA, Gardner, JPA and Bell, JJ (2013) Restriction of sponges to an atoll lagoon as a result of reduced environmental quality. Marine Pollution Bulletin 66, 209–220.CrossRefGoogle Scholar
Knapp, ISS, Williams, GJ and Bell, JJ (2016) Temporal dynamics and persistence of sponge assemblages in a Central Pacific atoll lagoon. Marine Ecology 37, 1147–1153.CrossRefGoogle Scholar
Kohler, KE and Gill, SM (2006) Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computational Geoscience 32, 1259–1269.CrossRefGoogle Scholar
Lamy, T, Galzin, R, Kulbicki, M, Lison de Loma, T and Claudet, J (2016) Three decades of recurrent declines and recoveries in corals belie ongoing change in fish assemblages. Coral Reefs 35, 293–302. .CrossRefGoogle Scholar
Lenth, R (2019) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.3.3. Available at https://CRAN.R-project.org/package=emmeans.Google Scholar
López-Victoria, M and Zea, S (2005) Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs. Marine Ecology 26, 33–41.CrossRefGoogle Scholar
López-Victoria, M, Zea, S and Weil, E (2006) Competition for space between encrusting excavating Caribbean sponges and other coral reef organisms. Marine Ecology Progress Series 312, 113–121.CrossRefGoogle Scholar
Marlow, J, Schönberg, CHL, Davy, SK, Haris, A, Jompa, J and Bell, JJ (2018 a) Bioeroding sponge assemblages: the importance of substrate availability and sediment. Journal of the Marine Biological Association of the United Kingdom 99, 343–358.CrossRefGoogle Scholar
Marlow, J, Smith, D, Werorilang, S and Bell, JJ (2018 b) Sedimentation limits the erosion rate of a bioeroding sponge. Marine Ecology 39, e12483.CrossRefGoogle Scholar
Marlow, J, Davy, SK, Shaffer, M, Haris, A and Bell, JJ (2018 c) Bleaching and recovery of a phototrophic bioeroding sponge. Coral Reefs 37, 565–570.CrossRefGoogle Scholar
Marlow, J, Haris, A, Jompa, J, Werorilangi, S, Bates, T, Bennett, H and Bell, JJ (2020) Spatial variation in the benthic community composition of coral reefs in the Wakatobi Marine National Park, Indonesia: updated baselines and limited benthic community shifts. Journal of the Marine Biological Association of the United Kingdom 100, 37–44.CrossRefGoogle Scholar
McMellor, S and Smith, DJ (2010) Coral reefs of the Wakatobi: abundance and biodiversity. In Clifton, J, Unsworth, R and Smith, DJ (eds), Marine Research and Conservation in the Coral Triangle: The Wakatobi Marine National Park. New York, NY: Nova Publishers, pp. 10–25.Google Scholar
Meissner, KJ, Lippmann, T and Sen Gupta, A (2012) Large-scale stress factors affecting coral reefs: open ocean sea surface temperature and surface seawater aragonite saturation over the next 400 years. Coral Reefs 31, 309–319.CrossRefGoogle Scholar
Mumby, PJ, Hastings, A and Edwards, HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450, 98–101.CrossRefGoogle ScholarPubMed
Negri, AP, Webster, NS, Hill, RT and Heyward, AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Marine Ecology Progress Series 223, 121–131.CrossRefGoogle Scholar
Norström, AV, Nyström, M, Lokrantz, J and Folke, C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Marine Ecology Progress Series 376, 293–306.CrossRefGoogle Scholar
Nurdin, N and Grydehøj, A (2014) Informal governance through patron-client relationships and destructive fishing in Spermonde Archipelago, Indonesia. Journal of Marine and Island Cultures 3, 54–59.CrossRefGoogle Scholar
O'Brien, JM and Scheibling, RE (2018) Turf wars: competition between foundation and turf-forming species on temperate and tropical reefs and its role in regime shifts. Marine Ecology Progress Series 590, 1–17.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2019) vegan: Community Ecology Package. Available at https://cran.r-project.org/package=vegan.Google Scholar
Pet-Soede, L and Erdmann, M (2003). Rapid Ecological Assessment Wakatobi National Park. Jakarta: Directorate General of Forest Protection and Nature Conservation, Ministry of Forestry; Denpasar, Bali: WWF Indonesia Marine Program; Bali: The Nature Conservancy, Southeast Asia Center for Marine Protected Areas.Google Scholar
Pinheiro, J, Bates, D, DebRoy, S and Sarkar, D and R Core Team (2018) nlme: Linear and Nonlinear Mixed Effects Models. Available at https://cran.r-project.org/package=nlme.Google Scholar
Plass-Johnson, JG, Heiden, JP, Abu, N, Lukman, M and Teichberg, M (2016) Experimental analysis of the effects of consumer exclusion on recruitment and succession of a coral reef system along a water quality gradient in the Spermonde Archipelago, Indonesia. Coral Reefs 35, 229–243.CrossRefGoogle Scholar
Polónia, ARM, Cleary, DFR, de Voogd, NJ, Renema, W, Hoeksema, BW, Martins, A and Gomes, NCM (2015) Habitat and water quality variables as predictors of community composition in an Indonesian coral reef: a multi-taxon study in the Spermonde Archipelago. Science of the Total Environment 537, 139–151.CrossRefGoogle Scholar
Powell, A, Smith, DJ, Hepburn, LJ, Jones, T, Berman, J, Jompa, J and Bell, JJ (2014) Reduced diversity and high sponge abundance on a sedimented Indo-Pacific reef system: implications for future changes in environmental quality. PLoS ONE 9, e85253.CrossRefGoogle ScholarPubMed
Qian, PY, Lau, SCK, Dahms, HU, Dobretsov, S and Harder, T (2007) Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Marine Biotechnology 9, 399–410.CrossRefGoogle ScholarPubMed
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at https://www.r-project.org/.Google Scholar
Ribeiro, B, Padua, A, Paiva, PC, Custódio, MR and Klautau, M (2018) Exploitation of micro refuges and epibiosis: survival strategies of a calcareous sponge. Journal of the Marine Biological Association of the United Kingdom 98, 495–503.CrossRefGoogle Scholar
Roberts, CM, Mittermeier, CG and Schueler, FW (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295, 1280–1285.CrossRefGoogle ScholarPubMed
Rogers, CS, Fitz HC, III, Gilnack, M, Beets, J and Hardin, J (1984) Scleractinian coral recruitment patterns at Salt River Submarine Canyon, St. Croix, US Virgin Islands. Coral Reefs 3, 69–76.CrossRefGoogle Scholar
Rovellini, A, Dunn, MR, Fulton, EA, Webster, NS, Smith, DJ, Jompa, J, Haris, A, Berman, J and Bell, JJ (2019) Decadal variability in sponge abundance and biodiversity on an Indo-Pacific coral reef. Marine Ecology Progress Series 620, 63–76.CrossRefGoogle Scholar
Rowley, SJ (2018) Environmental gradients structure gorgonian assemblages on coral reefs in SE Sulawesi, Indonesia. Coral Reefs 37, 609–630.CrossRefGoogle Scholar
Sawall, Y, Jompa, J, Litaay, M, Maddusila, A and Richter, C (2013) Coral recruitment and potential recovery of eutrophied and blast fishing impacted reefs in Spermonde Archipelago, Indonesia. Marine Pollution Bulletin 74, 374–382.CrossRefGoogle ScholarPubMed
Scheffer, M, Carpenter, S, Foley, JA, Folke, C and Walker, B (2001) Catastrophic shifts in ecosystems. Nature 413, 591–596.CrossRefGoogle ScholarPubMed
Schils, T (2012) Episodic eruptions of volcanic ash trigger a reversible cascade of nuisance species outbreaks in pristine coral habitats. PLoS ONE 7, e46639.CrossRefGoogle ScholarPubMed
Teichberg, M, Wild, C, Bednarz, VN, Kegler, HF, Lukman, M, Gärdes, AA, Heiden, JP, Weiand, L, Abu, N, Nasir, A, Miñarro, S, Ferse, SCA, Reuter, H and Plass-Johnson, JG (2018) Spatio-temporal patterns in coral reef communities of the Spermonde Archipelago, 2012–2014. I: comprehensive reef monitoring of water and benthic indicators reflect changes in reef health. Frontiers in Marine Science 5, 33.CrossRefGoogle Scholar
Warton, DI and Hui, FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 3–10.CrossRefGoogle ScholarPubMed
Whalan, S, Webster, NS and Negri, AP (2012) Crustose coralline algae and a cnidarian neuropeptide trigger larval settlement in two coral reef sponges. PLoS ONE 7, e30386.CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York, NY: Springer-Verlag.CrossRefGoogle Scholar
Wilson, JR, Ardiwijaya, RL and Prasetia, R (2012) A study of the impact of the 2010 coral bleaching event on coral communities in Wakatobi National Park. The Nature Conservancy, Indo-Pacific Division, Indonesia. Report No. 7/12.Google Scholar
Wulff, JL (2006) Ecological interactions of marine sponges. Canadian Journal of Zoology 84, 146–166.CrossRefGoogle Scholar
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