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Trait-based approach reveals how marginal reefs respond to acute and chronic disturbance

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Ecosystems worldwide are becoming increasingly altered by environmental stress, yet little is known about how acute disturbances affect ecological communities that already persist under chronically stressful environmental conditions. Here, we use a trait-based approach to understand the effects of repeated flooding on the subtropical reefs of Hervey Bay, Australia (25˚ South) that are considered marginal both in terms of their chronically turbid and high-latitude settings. We quantify variation in taxonomic and functional composition of coral assemblages along spatial gradients of water quality, before and after three flooding events of the Mary River between 2010 and 2013. We demonstrate systematic variation in taxonomic and functional composition along distance from shore and rivers and show remarkable stability of patterns over the course of repeated flooding. This is likely because the reefs of Hervey Bay are regularly exposed to resuspension of sediments, limiting the types of species that are able to persist in these chronically turbid settings, with flood events reinforcing the longer-term stress regime. Greater similarity of co-occurring species on nearshore reefs than expected by chance also supports this hypothesis. Corallite size, coral morphology, the ability to remove sediment, and propagule development rate best explained variation in coral assemblage structure. Specifically, reefs closer to shore and to rivers were characterised by species with large corallites, high sediment removal ability and foliose morphology, strategies considered beneficial in turbid conditions. Among individual traits, symbiont transmission best explained variation in assemblage structure, and it is plausible that the acquisition of locally adapted symbionts from the environment is advantageous in the turbid and light-limited conditions of nearshore reefs. These findings highlight the importance of tolerance to turbidity and sedimentation in driving coral biodiversity patterns in Hervey Bay, with acute flooding reinforcing the long-term stress regime that controls the distribution of species on these marginal reefs.

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References

  • Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253

    Article  PubMed  Google Scholar 

  • Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). Statistics Reference Online, Wiley StatsRef

    Book  Google Scholar 

  • Anthony KRN, Connolly SR (2004) Environmental limits to growth: physiological niche boundaries of corals along turbidity-light gradients. Oecologia 141:373–384

    Article  PubMed  Google Scholar 

  • Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471

    Article  Google Scholar 

  • Beger M, Sommer B, Harrison PL, Smith SDA, Pandolfi JM (2014) Conserving potential coral reef refuges at high latitudes. Divers Distrib 20:245–257

    Article  Google Scholar 

  • Berkelmans R, Jones A, Schaffelke B (2012) Salinity thresholds of Acropora spp. on the Great Barrier Reef. Coral Reefs:1–8

  • BOM (2011) Flood summary for the Mary River at Maryborough December 2010 - January 2011. Bureau of Meteorology, Australia

    Google Scholar 

  • Butler IR (2015) Flood response and palaeoecology of the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. PhD thesis, The University of Queensland

  • Butler IR, Sommer B, Zann M, Zhao JX, Pandolfi JM (2013) The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. Coral Reefs 32:1149–1163

    Article  Google Scholar 

  • Butler IR, Sommer B, Zann M, Zhao JX, Pandolfi JM (2015) The cumulative impacts of repeated heavy rainfall, flooding and altered water quality on the high-latitude coral reefs of Hervey Bay, Queensland, Australia. Mar Pollut Bull 96:356–367

    Article  CAS  PubMed  Google Scholar 

  • Case AL, Barrett SCH (2004) Environmental stress and the evolution of dioecy: Wurmbea dioica (Colchicaceae) in Western Australia. Evol Ecol 18:145–164

    Article  Google Scholar 

  • Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16:S101–S113

    Article  Google Scholar 

  • Conti-Jerpe IE, Thompson PD, Wong CWM, Oliveira NL, Duprey NN, Moynihan MA, Baker DM (2020) Trophic strategy and bleaching resistance in reef-building corals. Science Advances 6:eaaz5443

  • DeVantier LM (2010) Reef-building corals of Hervey Bay, South-East Queensland. Baseline survey report to the Wildlife Preservation Society of Queensland, Fraser Coast Branch

  • DeVantier LM, De’ath G, Turak E, Done TJ, Fabricius KE (2006) Species richness and community structure of reef-building corals on the nearshore great barrier reef. Coral Reefs 25:329–340

    Article  Google Scholar 

  • Devlin MJ, McKinna LW, Álvarez-Romero JG, Petus C, Abott B, Harkness P, Brodie J (2012) Mapping the pollutants in surface riverine flood plume waters in the great barrier reef, Australia. Mar Pollut Bull 65:224–235

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Zang R, Letcher SG, Liu S, He F (2012) Disturbance regime changes the trait distribution, phylogenetic structure and community assembly of tropical rain forests. Oikos 121:1263–1270

    Article  Google Scholar 

  • Done TJ (1982) Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1:95–107

    Article  Google Scholar 

  • Dornelas M (2010) Disturbance and change in biodiversity. Philos Trans R Soc Lond B Biol Sci 365:3719–3727

    Article  PubMed  PubMed Central  Google Scholar 

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  CAS  PubMed  Google Scholar 

  • Fabricius KE, Logan M, Weeks SJ, Lewis SE, Brodie J (2016) Changes in water clarity in response to river discharges on the Great Barrier Reef continental shelf: 2002–2013. Estuar Coast Shelf Sci 173:A1–A15

    Article  Google Scholar 

  • Figueiredo J, Baird AH, Connolly SR (2013) Synthesizing larval competence dynamics and reef-scale retention reveals a high potential for self-recruitment in corals. Ecology 94:650–659

    Article  PubMed  Google Scholar 

  • Flores F, Hoogenboom MO, Smith LD, Cooper TF, Abrego D, Negri AP (2012) Chronic exposure of corals to fine sediments: lethal and sub-lethal impacts. PLoS ONE 7:e37795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furnas MJ (2003) Catchments and corals: terrestrial runoff to the Great Barrier Reef. Australian Institute of Marine Science, Townsville, Queensland, Australia

    Google Scholar 

  • Gräwe U, Wolff JO, Ribbe J (2010) Impact of climate variability on an east Australian bay. Estuar Coast Shelf Sci 86:247–257

    Article  Google Scholar 

  • Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558

    Article  Google Scholar 

  • Harriott VJ, Banks SA (2002) Latitudinal variation in coral communities in eastern Australia: a qualitative biophysical model of factors regulating coral reefs. Coral Reefs 21:83–94

    Article  Google Scholar 

  • Hartmann AC, Baird AH, Knowlton N, Huang D (2017) The paradox of environmental symbiont acquisition in obligate mutualisms. Curr Biol 27:3711-3716.e3713

    Article  CAS  PubMed  Google Scholar 

  • Heidemann H, Ribbe J (2019) Marine heat waves and the influence of El Niño off Southeast Queensland. Aust Front Marine Sci 6:56

    Article  Google Scholar 

  • Hoogenboom MO, Connolly SR, Anthony KRN (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology 89:1144–1154

    Article  PubMed  Google Scholar 

  • Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    Article  PubMed  Google Scholar 

  • Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira W, Gilmour JP, Harrison HB, Heron S, 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, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Kerry JT, Connolly SR, Baird AH, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Jacobson M, Liu G, Pratchett MS, Skirving W, Torda G (2018a) Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat Climate Change 9(1):40–43

    Article  Google Scholar 

  • Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018b) Global warming transforms coral reef assemblages. Nature 556:492–496

    Article  CAS  PubMed  Google Scholar 

  • Johns KA, Osborne KO, Logan M (2014) Contrasting rates of coral recovery and reassembly in coral communities on the Great Barrier Reef. Coral Reefs 33:553–563

    Article  Google Scholar 

  • Jones AM, Berkelmans R (2014) Flood impacts in Keppel Bay, Southern great barrier reef in the aftermath of cyclonic rainfall. PLoS ONE 9:e84739

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones R, Fisher R, Bessell-Browne P (2019) Sediment deposition and coral smothering. PLoS ONE 14:e0216248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keith SA, Woolsey ES, Madin JS, Byrne M, Baird AH (2015) Differential establishment potential of species predicts a shift in coral assemblage structure across a biogeographic barrier. Ecography 38:1225–1234

    Article  Google Scholar 

  • Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960

    Article  PubMed  Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kim SW, Sampayo EM, Sommer B, Sims CA, Gomez-Cabrera MDC, Dalton SJ, Beger M, Malcolm HA, Ferrari R, Fraser N, Figueira WF, Smith SDA, Heron SF, Baird AH, Byrne M, Eakin CM, Edgar R, Hughes TP, Kyriacou N, Liu G, Matis PA, Skirving WJ, Pandolfi JM (2019) Refugia under threat: mass bleaching of coral assemblages in high-latitude eastern Australia. Glob Change Biol 25:3918–3931

    Article  Google Scholar 

  • Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits to coral reef development: Where do we draw the line? Am Zool 39:146–159

    Article  Google Scholar 

  • Kohler KE, 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. Comput Geosci 32:1259–1269

    Article  Google Scholar 

  • Kraft NJB, Adler PB, Godoy O, James EC, Fuller S, Levine JM (2015) Community assembly, coexistence and the environmental filtering metaphor. Funct Ecol 29:592–599

    Article  Google Scholar 

  • Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305

    Article  PubMed  Google Scholar 

  • Lavorel S, Grigulis K, McIntyre S, Williams NSG, Garden D, Dorrough J, Berman S, Quétier F, Thébault A, Bonis A (2008) Assessing functional diversity in the field–methodology matters! Funct Ecol 22:134–147

    Google Scholar 

  • Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24

    Article  Google Scholar 

  • Madin JS, Hoogenboom MO, Connolly SR, Darling ES, Falster DS, Huang D, Keith SA, Mizerek T, Pandolfi JM, Putnam HM, Baird AH (2016a) A trait-based approach to advance coral reef science. Trends Ecol Evol 31:419–428

    Article  PubMed  Google Scholar 

  • Madin JS, Anderson KD, Andreasen MH, Bridge TCL, Cairns SD, Connolly SR, Darling ES, Diaz M, Falster DS, Franklin EC, Gates RD, Hoogenboom MO, Huang D, Keith SA, Kosnik MA, Kuo C-Y, Lough JM, Lovelock CE, Luiz O, Martinelli J, Mizerek T, Pandolfi JM, Pochon X, Pratchett MS, Putnam HM, Roberts TE, Stat M, Wallace CC, Widman E, Baird AH (2016b) The coral trait database, a curated database of trait information for coral species from the global oceans. Sci Data 3:160017

    Article  PubMed  PubMed Central  Google Scholar 

  • McWilliam M, Pratchett MS, Hoogenboom MO, Hughes TP (2020) Deficits in functional trait diversity following recovery on coral reefs. Proceedings of the Royal Society B: Biological Sciences 287:20192628

  • Mellin C, Thompson A, Jonker MJ, Emslie MJ (2019) Cross-shelf variation in coral community response to disturbance on the great barrier reef. Diversity 11(3):38–53

    Article  Google Scholar 

  • Milbau A, Shevtsova A, Osler N, Mooshammer M, Graae BJ (2013) Plant community type and small-scale disturbances, but not altitude, influence the invasibility in subarctic ecosystems. New Phytol 197:1002–1011

    Article  PubMed  Google Scholar 

  • Mizerek TL, Baird AH, Beaumont LJ, Madin JS (2016) Environmental tolerance governs the presence of reef corals at latitudes beyond reef growth. Glob Ecol Biogeogr 25:979–987

    Article  Google Scholar 

  • Mouillot D, Graham NAJ, Villeger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177

    Article  PubMed  Google Scholar 

  • Muir PR, Wallace CC, Done T, Aguirre JD (2015) Limited scope for latitudinal extension of reef corals. Science 348:1135–1138

    Article  CAS  PubMed  Google Scholar 

  • Ng CSL, Huang D, Toh KB, Sam SQ, Kikuzawa YP, Toh TC, Taira D, Chan YKS, Hung LZT, Sim WT, Rashid AR, Afiq-Rosli L, Ng NK, Chou LM (2020) Responses of urban reef corals during the 2016 mass bleaching event. Mar Pollut Bull 154:111111

    Article  CAS  PubMed  Google Scholar 

  • Oksanan J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson G, Solymos P, Stevens MHH, Wagner H (2012) vegan: Community ecology package. R package version 2.0–5. http://cran.r-project.org/package=vegan

  • Ortiz J-C, Wolff NH, Anthony KRN, Devlin M, Lewis S, Mumby PJ (2018) Impaired recovery of the Great Barrier Reef under cumulative stress. Science Advances 4:eaar6127

  • Pandolfi JM, Lybolt M, Sommer B, Narayan R, Rachello-Dolmen P (2019) Coral and micro-benthic assemblages from reef habitats in Moreton Bay. In: Tibbetts IR, Rothlisberg PC, Neil DT, Homburg TA, Brewer DT, Arthington AH (eds) Moreton Bay Quandamooka & catchment: past, present, and future. The Moreton Bay Foundation, Brisbane, Australia, pp 361–377

    Google Scholar 

  • Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen IC, Clark TD, Colwell RK, Danielsen F, Evengård B, Falconi L, Ferrier S, Frusher S, Garcia RA, Griffis RB, Hobday AJ, Janion-Scheepers C, Jarzyna MA, Jennings S, Lenoir J, Linnetved HI, Martin VY, McCormack PC, McDonald J, Mitchell NJ, Mustonen T, Pandolfi JM, Pettorelli N, Popova E, Robinson SA, Scheffers BR, Shaw JD, Sorte CJB, Strugnell JM, Sunday JM, Tuanmu M-N, Vergés A, Villanueva C, Wernberg T, Wapstra E, Williams SE (2017) Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science 355:eaai9214

  • Perry CT, Larcombe P (2003) Marginal and non-reef-building coral environments. Coral Reefs 22:427–432

    Article  Google Scholar 

  • Pike N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2:278–282

    Article  Google Scholar 

  • Pinsky ML, Eikeset AM, McCauley DJ, Payne JL, Sunday JM (2019) Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569:108–111

    Article  CAS  PubMed  Google Scholar 

  • Pinzón CJH, Dornberger L, Beach-Letendre J, Weil E, Mydlarz LD (2014) The link between immunity and life history traits in scleractinian corals. PeerJ 2:e628

    Article  Google Scholar 

  • Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS ONE 9:e102498

    Article  PubMed  PubMed Central  Google Scholar 

  • Pratchett SM, Anderson DK, Hoogenboom OM, Widman E, Baird HA, Pandolfi MJ, Edmunds JP, Lough MJ (2015) Spatial, temporal and taxonomic variation in coral growth - implications for the structure and function of coral reef ecosystems. Oceanogr Mar Biol Annu Rev 53:215–295

    Google Scholar 

  • Pratchett MS, McWilliam MJ, Riegl B (2020) Contrasting shifts in coral assemblages with increasing disturbances. Coral Reefs 39(3):783–793

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, R Core Team, Vienna, Austria

    Google Scholar 

  • Radziejewska T (2002) Responses of deep-sea meiobenthic communities to sediment disturbance simulating effects of polymetallic nodule mining. Int Rev Hydrobiol 87:457–477

    Article  Google Scholar 

  • Richardson LE, Graham NAJ, Pratchett MS, Eurich JG, Hoey AS (2018) Mass coral bleaching causes biotic homogenization of reef fish assemblages. Glob Change Biol 24:3117–3129

    Article  Google Scholar 

  • Sommer B, Harrison PL, Beger M, Pandolfi JM (2014) Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:1000–1009

    Article  PubMed  Google Scholar 

  • Sommer B, Sampayo EM, Beger M, Harrison PL, Babcock RC, Pandolfi JM (2017) Local and regional controls of phylogenetic structure at the high-latitude range limits of corals. Proc R Soc Biol Sci Ser B 284

  • Sommer B, Beger M, Harrison PL, Babcock RC, Pandolfi JM (2018) Differential response to abiotic stress controls species distributions at biogeographic transition zones. Ecography 41:478–490

    Article  Google Scholar 

  • Stafford-Smith MG, Ormond RFG (1992) Sediment-rejection mechanisms of 42 species of Australian scleractinian corals. Aust J Mar Freshw Res 43:683–705

    Article  Google Scholar 

  • Villeger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301

    Article  PubMed  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Weiher E, Keddy PA (1995) Assembly rules, null models, and trait dispersion–new questions front old patterns. Oikos 74:159–164

    Article  Google Scholar 

  • Weiher E, Clarke GDP, Keddy PA (1998) Community assembly rules, morphological dispersion, and the coexistence of plant species. Oikos 81:309–322

    Article  Google Scholar 

  • Willis BL (1985) Phenotypic plasticity versus phenotypic stability in the reef corals Turbinaria mesenterina and Pavona cactus. Proceedings of the Fifth International Coral Reef Symposium 4:107–112

  • Wooldridge S, Brodie J, Furnas M (2006) Exposure of inner-shelf reefs to nutrient enriched runoff entering the great barrier reef lagoon: post-European changes and the design of water quality targets. Mar Pollut Bull 52:1467–1479

    Article  CAS  PubMed  Google Scholar 

  • Zawada KJA, Madin JS, Baird AH, Bridge TCL, Dornelas M (2019) Morphological traits can track coral reef responses to the Anthropocene. Funct Ecol 33:962–975

    Article  Google Scholar 

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Acknowledgements

We acknowledge support and funding from the Australian Research Council Centre of Excellence for Coral Reef Studies (CE0561435 and CE140100020), The University of Queensland, the National Environmental Research Program Tropical Ecosystems Hub Project 1.3, the Burnett Mary Regional Group and Reef Check Australia and The University of Sydney. We gratefully acknowledge generous field support from the staff of the Queensland Parks and Wildlife, Great Sandy Region, Hervey Bay, Queensland. Thanks also for field support from Tyson Martin, Andrew Olds, and Maria Beger.

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Sommer, B., Butler, I.R. & Pandolfi, J.M. Trait-based approach reveals how marginal reefs respond to acute and chronic disturbance. Coral Reefs 40, 735–749 (2021). https://doi.org/10.1007/s00338-021-02077-y

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