Abstract
Ecosystems are commonly affected by natural, episodic disturbances that can abruptly and drastically alter communities. Although it has been shown that resilient ecosystems can eventually recover to pre-disturbed states, the extent to which communities in early stages of recovery could be affected by multiple anthropogenic stressors is poorly understood. Pervasive and rising anthropogenic stressors in coastal marine systems that could interactively affect the recovery of these systems following natural disturbances include high sedimentation, nutrient enrichment, and overfishing. Using a 6-month field experiment, we examined the effects of all combinations of these three stressors on key functional groups in the benthic community growing on simulated, post-disturbance reef patches within a system recovering from large-scale natural disturbances (corallivorous seastar outbreak and cyclone). Our study revealed that sedimentation, nutrient enrichment, and overfishing (simulated using exclusion cages) interactively affected coral survival and algal growth, with taxon-specific effects at multiple scales. First, our treatments affected corals and algae differently, with sedimentation being more detrimental to macroalgal growth but less detrimental to coral (Porites rus) survival in caged plots, driving significant interactions between sedimentation and caging for both taxa. We also observed distinct responses between coral species and between algal functional groups, with the most extensive responses from algal turf biomass, for which sedimentation suppressed the synergistic (positive) combined effect of nutrient enrichment and caging. Our findings suggest that different combinations of ubiquitous anthropogenic stressors, related to either sea- or land-based activities, interactively influence community recovery from disturbance and may alter species compositions in the resulting community. Our findings further suggest that anthropogenic stressors could promote further degradation of coral reefs following natural disturbances by inhibiting recovery to coral-dominated states that provide vital ecosystem services to coastal populations worldwide.
References
Adjeroud M, Penin L, Carroll A (2007) Spatio-temporal heterogeneity in coral recruitment around Moorea, French Polynesia: implications for population maintenance. J Exp Mar Biol Ecol 341:204–218
Alldredge A (2012) MCR LTER: Coral Reef: Water column: Particle sedimentation on the forereef, back reef and fringing reef, http://metacat.lternet.edu/knb/metacat/knb-lter-mcr.12.15/lter
Alldredge A (2013) Moorea Coral Reef LTER: Coral reef: Water column: Nutrients, http://metacat.lternet.edu/knb/metacat/knb-lter-mcr.1034.7/lter
Ban SS, Graham NAJ, Connolly SR (2014) Evidence for multiple stressor interactions and effects on coral reefs. Glob Chang Biol 20:681–697
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193
Beldade R, Mills SC, Claudet J, Côté IM (2015) More coral, more fish? Contrasting snapshots from a remote Pacific atoll. PeerJ 3:e745
Bellwood DR, Fulton CJ (2008) Sediment-mediated suppression of herbivory on coral reefs: decreasing resilience to rising sea levels and climate change? Limnol Oceanogr 53:2695–2701
Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833
Birrell C, McCook L, Willis B (2005) Effects of algal turfs and sediment on coral settlement. Mar Pollut Bull 51:408–414
Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460
Bulleri F, Couraudon-Réale M, Lison de Loma T, Claudet J (2013) Variability in the effects of macroalgae on the survival and growth of corals: the consumer connection. PLoS One 8:e79712
Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139
Burkepile DE, Hay ME (2009) Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Mar Ecol Prog Ser 389:71–84
Chazdon RL (2003) Tropical forest recovery: legacies of human impact and natural disturbances. Perspect Plant Ecol Evol Syst 6:51–71
Connell JH (1978) Diversity in tropical rain forests and coral reefs: high diversity of trees and corals is maintained only in a non-equilibrium state. Science 199:1302–1310
Connell SD, Russell BD, Turner DJ, Shepherd SA, Kildea T, Miller D, Airoldi L, Cheshire A (2008) Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar Ecol Prog Ser 360:63–72
Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315
Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286
Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Cote IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386
Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395
De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109:17995–17999
Dilley M, Chen RS, Deichmann U, Lerner-Lam AL, Arnold M, Agwe J, Buys P, Kjevstad O, Lyon B, Yetman G (2005) Natural disaster hotspots: a global risk analysis. The World Bank, Washington, D.C.
Dulvy NK, Freckleton RP, Polunin NVC (2004) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416
Dunn JG, Sammarco PW, LaFleur G (2012) Effects of phosphate on growth and skeletal density in the scleractinian coral Acropora muricata: A controlled experimental approach. J Exp Mar Biol Ecol 411:34–44
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142
Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: A review. Mar Pollut Bull 64:1737–1765
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146
Fabricius KE (2011) Factors determining the resilience of coral reefs to eutrophication: A review and conceptual model. Springer, Dordrecht, Netherlands
Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574
Fong P, Paul VJ (2011) Coral reef algae. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition, pp 241–272
Foster DR, Fluet M, Boose ER (1999) Human or natural disturbance: Landscape-scale dynamics of the tropical forests of Puerto Rico. Ecol Appl 9:555–572
Gil MA (2013) Unity through nonlinearity: a unimodal coral–nutrient interaction. Ecology 94:1871–1877
Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71
Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97
Grigg RW (1995) Coral reefs in an urban embayment in Hawaii: A complex case history controlled by natural and anthropogenic stress. Coral Reefs 14:253–266
Halpern B, McLeod K, Rosenberg A, Crowder L (2008) Managing for cumulative impacts in ecosystem-based management through ocean zoning. Ocean Coast Manage 51:203–211
Halpern BS, Selkoe KA, White C, Albert S, Aswani S, Lauer M (2012) Marine protected areas and resilience to sedimentation in the Solomon Islands. Coral Reefs 32:61–69
Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition, pp 59–85
Hayne M, Chappell J (2001) Cyclone frequency during the last 5000 years at Curacoa Island, north Queensland, Australia. Palaeogeography Palaeoclimatology Palaeoecology 168:207–219
Hench JL, Leichter JJ, Monismith SG (2008) Episodic circulation and exchange in a wave-driven coral reef and lagoon system. Limnol Oceanogr 53:2681–2694
Hoegh-Guldberg O, Smith GJ (1989) Influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Mar Ecol Prog Ser 57:173–186
Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638
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
Jokiel PL, Rodgers KS, Storlazzi CD, Field ME, Lager CV, Lager D (2014) Response of reef corals on a fringing reef flat to elevated suspended-sediment concentrations: Moloka‘i. Hawai‘i. PeerJ 2:e699
Jones HP, Schmitz OJ (2009) Rapid recovery of damaged ecosystems. PLoS ONE 4:e5653
Koop K, Booth D, Broadbent A, Brodie J, Bucher D, Capone D, Coll J, Dennison W, Erdmann M, Harrison P, Hoegh-Guldberg O, Hutchings P, Jones GB, Larkum AWD, O’Neil J, Steven A, Tentori E, Ward S, Williamson J, Yellowlees D (2001) ENCORE: The effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar Pollut Bull 42:91–120
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 323:107–117
Lamy T, Galzin R, Kulbicki M, Lison de Loma T, Claudet J (2016) Three decades of recurrent declines and recoveries in corals belie ongoing change in fish assemblages. Coral Reefs 35:293–302
Lapointe BE, Langton R, Bedford BJ, Potts AC, Day O, Hu C (2010) Land-based nutrient enrichment of the Buccoo Reef Complex and fringing coral reefs of Tobago, West Indies. Mar Pollut Bull 60:334–343
Leenhardt P, Lauer M, Madi Moussa R, Holbrook SJ, Rassweiler A, Schmitt RJ, Claudet J (2016) Complexities and uncertainties in transitioning small-scale coral reef fisheries. Frontiers in Marine Science. doi:10.3389/fmars.2016.00070
Leichter JJ, Aildredge AL, Bernardi G, Brooks AJ, Carlson CA, Carpenter RC, Edmunds PJ, Fewing MR, Hanson KM, Hench JL, Holbrook SJ, Nelson CE, Toonen RJ, Shburn LW, Wyatt ASJ (2013) Biological and physical interactions on a tropical island coral reef - transport and retention processes on Moorea, French Polynesia. Oceanography 26:52–63
Lenihan HS, Holbrook SJ, Schmitt RJ, Brooks AJ (2011) Influence of corallivory, competition, and habitat structure on coral community shifts. Ecology 92:1959–1971
Lenihan HS, Hench JL, Holbrook SJ, Schmitt RJ, Potoski M (2015) Hydrodynamics influence coral performance through simultaneous direct and indirect effects. Ecology 96:1540–1549
Leray M, Béraud M, Anker A, Chancerelle Y, Mills SC (2012) Acanthaster planci outbreak: Decline in coral health, coral size structure modification and consequences for obligate decapod assemblages. PLoS One 7:e35456
Levin SA, Paine RT (1974) Disturbance, patch formation, and community structure. Proc Natl Acad Sci USA 71:2744–2747
Littler MM, Littler DS (2007) Assessment of coral reefs using herbivory/nutrient assays and indicator groups of benthic primary producers: a critical synthesis, proposed protocols, and critique of management strategies. Aquat Conserv 17:195–215
Littler M, Littler D, Brooks B (2006) Harmful algae on tropical coral reefs: Bottom-up eutrophication and top-down herbivory. Harmful Algae 5:565–585
Madin JS, Baird AH, Dornelas M, Connolly SR (2014) Mechanical vulnerability explains size-dependent mortality of reef corals. Ecol Lett 17:1008–1015
McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367
McCook LJ, 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
Mills SC (2012) Density-dependent prophylaxis in the coral-eating crown-of-thorns sea star, Acanthaster planci. Coral Reefs 31:603–612
Muthukrishnan R, Fong P (2014) Multiple anthropogenic stressors exert complex, interactive effects on a coral reef community. Coral Reefs 33:911–921
Nugues MM, Roberts CM (2003) Coral mortality and interaction with algae in relation to sedimentation. Coral Reefs 22:507–516
Nyström M (2006) Redundancy and response diversity of functional groups: implications for the resilience of coral reefs. Ambio 35:30–35
Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417
Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996
Penin L, Michonneau F, Baird AH, Connolly SR, Pratchett MS, Kayal M, Adjeroud M (2010) Early post-settlement mortality and the structure of coral assemblages. Mar Ecol Prog Ser 408:55–64
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107:9683–9688
Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202
Ruppert JLW, Travers MJ, Smith LL, Fortin M-J, Meekan MG (2013) Caught in the middle: combined impacts of shark removal and coral loss on the fish communities of coral reefs. PLoS One 8:e74648
Short FT, Wyllie-Echeverria S (1996) Natural and human-induced disturbance of seagrasses. Environ Conserv 23:17–27
Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9:835–845
Veron JEN (1995) Corals in space and time: The biogeography and evolution of the Scleractinia. University of New South Wales Press, Sydney, Australia
Wartian MJ (2006) Determinants of community structure and resilience on tropical eastern Pacific coral reefs. University of California Los Angeles, pp 60–111
Wheeler B (2010) lmPerm: Permutation tests for linear models
Wielgus J, Chadwick-Furman NE, Dubinsky Z (2004) Coral cover and partial mortality on anthropogenically impacted coral reefs at Eilat, northern Red Sea. Mar Pollut Bull 48:248–253
Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790
Acknowledgments
We thank L. Jacobson, M. Adjeroud, C. Fuchs, P. Leenhardt, F. Lerouvreur, J. Zill, the staffs of CRIOBE and the Richard B. Gump South Pacific Research Station for logistical support, and C.W. Osenberg, R.F. Fletcher, and G. Paulay for constructive comments on previous versions of this manuscript. Funding for this work was provided by the Embassy of France in the United States (Chateaubriand Fellowship awarded to M.A.G.), the National Science Foundation (Graduate Research [DGE-802270] and Postdoctoral Research [1523875] Fellowships awarded to M.A.G. and grant OCE-1130359), Florida Sea Grant (fellowship awarded to M.A.G.), the Agence Nationale de la Recherche (ANR-11-JSV7-012-01 LIVE AND LET DIE awarded to S.C.M. and J.C. and ANR-14-CE03-0001-01 ACRoSS awarded to J.C.), the Partnership University Fund of the French American Cultural Exchange (Ocean Bridges Program, http://facecouncil.org/puf/ awarded to S.C.M.), and the Fondation de France (INTHENSE project awarded to J.C.).
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Gil, M.A., Goldenberg, S.U., Ly Thai Bach, A. et al. Interactive effects of three pervasive marine stressors in a post-disturbance coral reef. Coral Reefs 35, 1281–1293 (2016). https://doi.org/10.1007/s00338-016-1489-x
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DOI: https://doi.org/10.1007/s00338-016-1489-x