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Resilience of the Marine Animal Forest: Lessons from Maldivian Coral Reefs After the Mass Mortality of 1998

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Marine Animal Forests

Abstract

Resilience is the ability of the ecosystem to recover after a perturbation. Assessing the resilience of marine ecosystems in the face of the increasing disturbance regime has become a major concern for their conservation. Among marine ecosystems, animal forests are expectedly little resilient. Their recovery may take long, increasing the risk of hysteresis and phase shift. Historical data series for most animal forests are virtually inexistent due to the challenging difficulty of the study of deep- and cold-water habitats. Tropical coral reefs, thriving in warm shallow waters, have undoubtedly been the best studied example of animal forest for a long time and may therefore provide ideas and concepts to be applied to the study of other animal forests. In this chapter, a historical data series on the coral reefs of the Maldives, which suffered mass mortality following the bleaching caused by the extreme El Niño – Southern Oscillation (ENSO) episode of 1998, is analyzed using an array of different descriptors to measure resilience. According to the specific descriptor considered, resilience varied between 4 and 16+ years, but full recovery may even be considered unachieved, as there are species that have not come back yet. The main take-home message from this Maldivian example is the need of adopting several distinct descriptors to assess the resilience of animal forests. Concentrating on the demography of the dominant species is not sufficient to get a reliable measure of whole ecosystem resilience.

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References

  • Andréfouët S, editor. Biodiversity, resources, and conservation of Baa Atoll (Republic of Maldives): a UNESCO man and biosphere reserve. Atoll Res Bull. 2012;590:1–235.

    Google Scholar 

  • Bianchi CN. Climate change and biological response in the marine benthos. Proc Ital Assoc Oceanol Limnol. 1997;12(1):3–20.

    Google Scholar 

  • Bianchi CN. Bioconstruction in marine ecosystems and Italian marine biology. Biol Mar Mediterr. 2001;8:112–30.

    Google Scholar 

  • Bianchi CN, Colantoni P, Geister J, Morri C. Reef geomorphology, sediments and ecological zonation at Felidu Atoll, Maldive Islands (Indian Ocean). In: Lessios HA, MacIntyre IG, editors. Proceedings of the 8th International Coral Reef Symposium, vol. 1. Panamá: Smithsonian Tropical Research Institute; 1997. p. 431–6.

    Google Scholar 

  • Bianchi CN, Pichon M, Morri C, Colantoni P, Benzoni F, Baldelli G, Sandrini M. Le suivi du blanchissement des coraux aux Maldives: leçons à tirer et nouvelles hypothèses. Oceanis. 2003;29(3–4):325–54.

    Google Scholar 

  • Bianchi CN, Pronzato R, Cattaneo-Vietti R, Benedetti-Cecchi L, Morri C, Pansini M, Chemello R, Milazzo M, Fraschetti S, Terlizzi A, Peirano A, Salvati E, Benzoni F, Calcinai B, Cerrano C, Bavestrello G. Hard bottoms. Biol Mar Mediterr. 2004;11 Suppl 1:185–215.

    Google Scholar 

  • Bianchi CN, Catra M, Giaccone G, Morri C. Il paesaggio marino costiero: ambienti e diversità. In: Cosentino A, La Posta A, Maggiore AM, Tartaglini N, editors. Mediterraneo: ambienti, paesaggio, diversità. Milano: Téchne; 2005. p. 30–61.

    Google Scholar 

  • Bianchi CN, Morri C, Pichon M, Benzoni F, Colantoni P, Baldelli G, Sandrini M. Dynamics and pattern of coral recolonization following the 1998 bleaching event in the reefs of the Maldives. In: Suzuki Y, Nakamori T, Hidaka M, Kayanne H, Casareto BE, Nadaoka K, Yamano H, Tsuchiya M, editors. Proceedings of the 10th International Coral Reef Symposium. Tokyo: Japanese Coral Reef Society; 2006. p. 30–7.

    Google Scholar 

  • Bianchi CN, Morri C, Chiantore M, Montefalcone M, Parravicini V, Rovere A. Mediterranean Sea biodiversity between the legacy from the past and a future of change. In: Stambler N, editor. Life in the Mediterranean Sea: a look at habitat changes. New York: Nova; 2012. p. 1–55.

    Google Scholar 

  • Bigot L, Amir H. Scleractinia corals of Baa Atoll (Maldives): first check list and overview of stony corals community structure. Atoll Res Bull. 2012;590:67–83.

    Google Scholar 

  • Black KP, Moran PJ, Hammond LS. Numerical-models show coral reefs can be self-seeding. Mar Ecol Prog Ser. 1991;74(1):1–11.

    Article  Google Scholar 

  • Bo M, Bavestrello G, Angiolillo M, Calcagnile L, Canese S, Cannas R, Cau A, D’Elia M, D’Oriano F, Follesa MC, Quarta G, Cau A. Persistence of pristine deep-sea coral gardens in the Mediterranean Sea (SW Sardinia). PLoS One. 2015;10(3):e0119393.

    Article  PubMed  PubMed Central  Google Scholar 

  • Boström C, Pittman SJ, Simenstad C, Kneib RT. Seascape ecology of coastal biogenic habitats: advances, gaps, and challenges. Mar Ecol Prog Ser. 2011;427:191–217.

    Article  Google Scholar 

  • Boudouresque CF, Ruitton S, Bianchi CN, Chevaldonné P, Fernandez C, Harmelin-Vivien M, Ourgaud M, Pasqualini V, Perez T, Pergent G, Thibaut T, Verlaque M. Terrestrial versus marine diversity of ecosystems. And the winner is: the marine realm. In: Langar H, Bouafif C, Ouerghi A, editors. Proceedings of the 5th Mediterranean symposium on marine vegetation. Tunis: UNEP/MAP–RAC/SPA; 2014. p. 11–25.

    Google Scholar 

  • Calcinai B, Bavestrello G, Cerrano C. Dispersal and association of two alien species in the Indonesian coral reefs: the octocoral Carijoa riisei and the demosponge Desmapsamma anchorata. J Mar Biol Assoc UK. 2004;84(5):937–41.

    Article  Google Scholar 

  • Cardini U, Chiantore M, Lasagna R, Morri C, Bianchi CN. Size-structure patterns of juvenile hard corals in the Maldives. J Mar Biol Assoc UK. 2012;92(6):1335–9.

    Article  Google Scholar 

  • Cheal AJ, MacNeil MA, Cripps E, Emslie MJ, Jonker M, Schaffelke B, Sweatman H. Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs. 2010;29:1005–15.

    Article  Google Scholar 

  • Ciarapica G, Passeri L. An overview of the Maldivian coral reefs in Felidu and North Malé atolls (Indian Ocean): platform drowning by ecological crises. Facies. 1993;28:33–66.

    Article  Google Scholar 

  • Cocito S, Ferdeghini F, Morri C, Bianchi CN. Patterns of bioconstruction in the cheilostome bryozoan Schizoporella errata: the influence of hydrodynamics and associated biota. Mar Ecol Prog Ser. 2000;192:153–61.

    Article  Google Scholar 

  • Côté IM, Darling ES. Rethinking ecosystem resilience in the face of climate change. PLoS Biol. 2010;8:e1000438.

    Article  PubMed  PubMed Central  Google Scholar 

  • Duarte CM, Borja Á, Carstensen J, Elliott M, Krause-Jensen D, Marbà N. Paradigms in the recovery of estuarine and coastal ecosystems. Estuar Coasts. 2015;38:1202–12.

    Article  Google Scholar 

  • Ferrigno F, Bianchi CN, Lasagna R, Morri C, Russo GF, Sandulli R. Corals in high diversity reefs resist human impact. Ecol Indic. 2016;70:106–13.

    Article  Google Scholar 

  • Gatti G, Montefalcone M, Rovere A, Parravicini V, Morri C, Albertelli G, Bianchi CN. Seafloor integrity down the harbor waterfront: the coralligenous shoals off Vado Ligure (NW Mediterranean). Adv Oceanogr Limnol. 2012;3(1):51–67.

    Article  Google Scholar 

  • Gatti G, Bianchi CN, Parravicini V, Rovere A, Peirano A, Montefalcone M, Massa F, Morri C. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS One. 2015a;10(2):e0118581.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gatti G, Bianchi CN, Morri C, Montefalcone M, Sartoretto S. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecol Indic. 2015b;52:567–76.

    Article  Google Scholar 

  • Glynn PW. Bioerosion and coral-reef growth: a dynamic balance. In: Birkeland C, editor. Life and death of coral reefs. New York: Chapman & Hall; 1997. p. 68–95.

    Chapter  Google Scholar 

  • Graham NAJ, Chong-Seng KM, Huchery C, Januchowski-Hartley FA, Nash KL. Coral reef community composition in the context of disturbance history on the Great Barrier Reef, Australia. PLoS One. 2014;9(7):e101204.

    Article  PubMed  PubMed Central  Google Scholar 

  • Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature. 2015;518(7537):94–7.

    Article  CAS  PubMed  Google Scholar 

  • Gravier-Bonnet N, Bourmaud C. Hydroids (Cnidaria, Hydrozoa) of Baa Atoll (Indian Ocean, Maldives Archipelago). Atoll Res Bull. 2012;590:85–123.

    Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke CS, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J. Climate change, human impacts, and the resilience of coral reefs. Science. 2003;301:929–33.

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Bellwood DR, Folke CS, Steneck RS, Wilson J. New paradigms for supporting the resilience of marine ecosystems. Trends Ecol Evol. 2005;20(7):380–6.

    Article  PubMed  Google Scholar 

  • Hughes TP, Bellwood DR, Folke CS, McCook LJ, Pandolfi JM. No-take areas, herbivory and coral reef resilience. Trends Ecol Evol. 2007a;22(1):1–3.

    Article  PubMed  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol. 2007b;17:360–5.

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS. Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol. 2010;25(11):633–42.

    Article  PubMed  Google Scholar 

  • Hutchings PA. Biological destruction of coral reefs. Coral Reefs. 1986;4:239–52.

    Article  Google Scholar 

  • Jimenez H, Bigot L, Bourmaud C, Chabanet P, Gravier-Bonnet N, Hamel MA, Payri C, Mattio L, Menou JL, Naeem S, Rilwan Y, Sattar S, Scott L, Shiham A, Vigliola L, Andréfouët S. Multi-taxa coral reef community structure in relation to habitats in the Baa Atoll Man and Biosphere UNESCO Reserve (Maldives), and implications for its conservation. J Sea Res. 2012;72:77–86.

    Article  Google Scholar 

  • Jokiel PL. How corals gain foothold in new environments. Coral Reefs. 1992;11(4):192.

    Article  Google Scholar 

  • Lasagna R, Gattorna I, Albertelli G, Morri C, Bianchi CN. Substrate heterogeneity and relation with coral recruitment in coral reefs of the Maldives (Indian Ocean). Biol Mar Mediterr. 2006;13(2):88–9.

    Google Scholar 

  • Lasagna R, Albertelli G, Giovannetti E, Grondona M, Milani A, Morri C, Bianchi CN. Status of Maldivian reefs eight years after the 1998 coral mass mortality. Chem Ecol. 2008;24(S1):155–60.

    Google Scholar 

  • Lasagna R, Albertelli G, Morri C, Bianchi CN. Acropora abundance and size in the Maldives six years after the 1998 mass mortality: patterns across reef typologies and depths. J Mar Biol Assoc UK. 2010a;90(5):919–22.

    Article  Google Scholar 

  • Lasagna R, Albertelli G, Colantoni P, Morri C, Bianchi CN. Ecological stages of Maldivian reefs after the coral mass mortality of 1998. Facies. 2010b;56(1):1–11.

    Article  Google Scholar 

  • Lasagna R, Gnone G, Taruffi M, Morri C, Bianchi CN, Parravicini V, Lavorano S. A new synthetic index to evaluate reef coral condition. Ecol Indic. 2014;40:100–10.

    Article  Google Scholar 

  • Lotze HK, Coll M, Magera AM, Ward-Paige C, Airoldi L. Recovery of marine animal populations and ecosystems. Trends Ecol Evol. 2011;26(11):595–605.

    Article  PubMed  Google Scholar 

  • Martínez-Rendis A, Acosta González G, Luis Hernández-Stefanoni J, Arias González JE. Quantifying the reefscape transformation of a coastal Caribbean coral reef during a phase shift and the associated coastal landscape change. Mar Ecol. 2016;37(3):697–710.

    Google Scholar 

  • McMurray SE, Blum JE, Pawlik JR. Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. Mar Biol. 2008;155:159–71.

    Article  Google Scholar 

  • Montefalcone M, Parravicini V, Bianchi CN. Quantification of coastal ecosystem resilience. In: Wolanski E, McLusky DS, editors. Treatise on estuarine and coastal science, Ecohydrology and Restoration, vol. 10. Waltham: Elsevier/Academic Press; 2011. p. 49–70.

    Chapter  Google Scholar 

  • Morri C, Bianchi CN. Ecological niches of hermatypic corals at Ilha do Sal (Arquipélago de Cabo Verde). Bol Museu Municipal do Funchal. 1995;4 Suppl:473–85.

    Google Scholar 

  • Morri C, Bianchi CN, Aliani S. Coral reefs at Gangehi (North Ari Atoll, Maldive Islands). Publ Serv Géologique du Luxembourg. 1995;29:3–12.

    Google Scholar 

  • Morri C, Aliani S, Bianchi CN. Reef status in the Rasfari region (North Malé Atoll, Maldives) five years before the mass mortality event of 1998. Estuar Coast Shelf Sci. 2010;86(2):258–64.

    Article  Google Scholar 

  • Morri C, Montefalcone M, Lasagna R, Gatti G, Rovere A, Parravicini V, Baldelli G, Colantoni P, Bianchi CN. Through bleaching and tsunami: coral reef recovery in the Maldives. Mar Pollut Bull. 2015;98:188–200.

    Article  CAS  PubMed  Google Scholar 

  • Mumby PJ, Hastings A, Edwards HJ. Thresholds and the resilience of Caribbean coral reefs. Nature. 2007;450:98–101.

    Article  CAS  PubMed  Google Scholar 

  • Nepote E, Bianchi CN, Chiantore M, Morri C, Montefalcone M. Pattern and intensity of human impact on coral reefs depend on depth along the reef profile and on the descriptor adopted. Estuar Coast Shelf Sci. 2016;178:86–91.

    Google Scholar 

  • Nyström M, Folke C. Spatial resilience of coral reefs. Ecosystems. 2001;4:406–17.

    Article  Google Scholar 

  • Nyström M, Folke C, Moberg F. Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol. 2000;15(10):413–7.

    Article  PubMed  Google Scholar 

  • Nyström M, Graham NAJ, Lokrantz J, Norström AV. Capturing the cornerstones of coral reef resilience: linking theory to practice. Coral Reefs. 2008;27:795–809.

    Article  Google Scholar 

  • Obura DO. Resilience and climate change: lessons from coral reefs and bleaching in the Western Indian Ocean. Estuar Coast Shelf Sci. 2005;63:353–72.

    Article  Google Scholar 

  • Parrish FA, Roark EB. Growth validation of gold coral Gerardia sp. in the Hawaiian Archipelago. Mar Ecol Prog Ser. 2009;397:163–72.

    Article  Google Scholar 

  • Pichon M, Benzoni F. Taxonomic re-appraisal of zooxanthellate scleractinian corals in the Maldive Archipelago. Zootaxa. 2007;1441:21–33.

    Article  Google Scholar 

  • Pillai CSG. The distribution of shallow-water stony corals at Minicoy atoll in the Indian Ocean with a check-list of species. Atoll Res Bull. 1971;141:1–12.

    Google Scholar 

  • Pillai CSG. Stony corals of the seas around India. In: Mukundan C, Pillai CSG, editors. Proceedings of the First International Symposium on Corals and Coral Reefs. Mandapam Camp: Marine Biological Association of India; 1972. p. 191–216.

    Google Scholar 

  • Pillai CSG, Scheer G. Report on the stony corals from the Maldive Archipelago. Zoologica. 1976;43(3–126):1–83.

    Google Scholar 

  • Pittman S, Kneib R, Simenstad C, Nagelkerken I, editors. Seascape ecology: application of landscape ecology to the marine environment. Mar Ecol Prog Ser. 2011;427:187–90.

    Google Scholar 

  • Rossi S. El planeta azul: un universo en extinción. Barcelona: Debate; 2011. 428 pp.

    Google Scholar 

  • Rossi S. The destruction of the ‘animal forests’ in the oceans: towards an over-simplification of the benthic ecosystems. Ocean Coast Manag. 2013;84:77–85.

    Article  Google Scholar 

  • Rovere A, Parravicini V, Firpo M, Morri C, Bianchi CN. Combining geomorphologic, biological and accessibility values for marine natural heritage evaluation and conservation. Aquat Conserv Mar Freshwat Ecosyst. 2011;21:541–52.

    Article  Google Scholar 

  • Rowlands G, Purkis S, Bruckner A. Tight coupling between coral reef morphology and mapped resilience in the Red Sea. Mar Pollut Bull. 2016;105(2):575–85.

    Google Scholar 

  • Sammarco PW, Andrews JC. Localized dispersal and recruitment in Great Barrier Reef corals: the Helix experiment. Science. 1988;239(4846):1422–4.

    Article  CAS  PubMed  Google Scholar 

  • Sammarco PW, Porter SA, Cairns SD. A new coral species introduced into the Atlantic Ocean – Tubastraea micranthus (Ehrenberg, 1834) (Cnidaria, Anthozoa, Scleractinia): an invasive threat. Aquat Invasions. 2010;5(2):131–40.

    Article  Google Scholar 

  • Santangelo G, Cupido R, Cocito S, Bramanti L, Priori C, Erra F, Iannelli M. Effects of increased mortality on gorgonian corals (Cnidaria, Octocorallia): different demographic features may lead affected populations to unexpected recovery and new equilibrium points. Hydrobiologia. 2015;759(1):171–87.

    Google Scholar 

  • Schlacher TA, Rowden AA, Dower JF, Consalvey M. Seamount science scales undersea mountains: new research and outlook. Mar Ecol. 2010;31 Suppl 1:1–13.

    Article  Google Scholar 

  • Schuhmacher H, Zibrowius H. What is hermatypic? A redefinition of ecological groups in corals and other organisms. Coral Reefs. 1984;4:1–9.

    Article  Google Scholar 

  • Schuhmacher H, Loch W, Loch K. Post-bleaching growth reveals Diploastrea heliopora to be a coral methusalem. Coral Reefs. 2002;21:344–5. + Erratum 22: 88, 2003.

    Google Scholar 

  • Sheppard CRC. Coral species of the Indian Ocean and adjacent seas: a synonymized compilation and some regional distributional patterns. Atoll Res Bull. 1987;307:1–32.

    Article  Google Scholar 

  • Standish RJ, Hobbs RJ, Mayfield MM, Bestelmeyer BT, Suding KN, Battaglia LL, Eviner V, Hawkes CV, Temperton VM, Cramer VA, Harris JA, Funk JL, Thomas PA. Resilience in ecology: abstraction, distraction, or where the action is? Biol Conserv. 2014;177:43–51.

    Article  Google Scholar 

  • Teixidó N, Garrabou J, Harmelin JG. Low dynamics, high longevity and persistence of sessile structural species dwelling on Mediterranean coralligenous outcrops. PLoS One. 2011;6(8):e23744.

    Article  PubMed  PubMed Central  Google Scholar 

  • Veron JEN. Corals of the world, vol. 3. Townsville: Australian Institute of Marine Science; 2000.

    Google Scholar 

  • Wallace CC, Zahir H. The ‘Xarifa’ expedition and the atolls of the Maldives, 50 years on. Coral Reefs. 2007;26:3–5.

    Article  Google Scholar 

  • Wells JW, Spencer-Davies P. Preliminary list of stony corals from Addu Atoll. Atoll Res Bull. 1966;116:43–55.

    Google Scholar 

  • West JM, Salm RV. Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol. 2003;17(4):956–67.

    Article  Google Scholar 

  • Williams A, Schlacher TA, Rowden AA, Althaus F, Clark MR, Bowden DA, Stewart R, Bax NJ, Consalvey M, Kloser RJ. Seamount megabenthic assemblages fail to recover from trawling impacts. Mar Ecol. 2010;31 Suppl 1:183–99.

    Article  Google Scholar 

  • Yap HT. Coral reef resilience. Mar Pollut Bull. 2007;54:1075–6.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Lorenzo “Loran” Bramanti (Banyuls sur mer, France) for his kind invitation to write this chapter. Albatros Top Boat (Verbania and Milan, Italy, and Malé, Maldives) organized our scientific cruises in the Maldives. We especially thank Donatella “Dodi” Telli and Massimo Sandrini for their support. We wish to dedicate this chapter to the great Italian marine scientist Paolo Colantoni (1934–2015), who fostered our research in the Maldives and has been both a master and friend to all of us.

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Bianchi, C.N. et al. (2017). Resilience of the Marine Animal Forest: Lessons from Maldivian Coral Reefs After the Mass Mortality of 1998. In: Rossi, S., Bramanti, L., Gori, A., Orejas , C. (eds) Marine Animal Forests. Springer, Cham. https://doi.org/10.1007/978-3-319-21012-4_35

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