Abstract
Indonesian coral reefs are the epicenter of marine biodiversity, yet are under rapid anthropogenically induced decline. Therefore, ecological monitoring of high diversity taxa is paramount to facilitate effective management and conservation. This study presents an initial report from a comprehensive survey of shallow-water (0–15 m) gorgonian assemblage composition and structure across sites with varying habitat quality within the Wakatobi Marine National Park (WMNP), SE Sulawesi, Indonesia. Current estimates of over 90 morphospecies from 38 genera and 12 families within the calcaxonian, holaxonian and scleraxonian groups are reported. This extensive survey confirms high local gorgonian abundance, diversity and species richness in the absence of anthropogenic influence and increasing with depth. Notably, morphological variants of the zooxanthellate species Isis hippuris Linnaeus, 1758, and Briareum Blainville, 1830, drive site and habitat assemblage differences across environmental gradients. Azooxanthellate taxa, particularly within the Plexauridae, drive species richness and diversity with depth. Of the 14 predictor variables measured, benthic characteristics, water flow and natural light explained just 30% of gorgonian assemblage structure. Furthermore, zooxanthellate and azooxanthellate taxa partitioned distinct gorgonian communities into two trophic groups—autotrophs and heterotrophs, respectively—with contrasting diversity and abundance patterns within and between study sites. This study strongly supports the WMNP as an area of high regional gorgonian abundance and diversity. Varying ecological patterns across environmental clines can provide the foundation for future research and conservation management strategies in some of the most biodiverse marine ecosystems in the world.
Similar content being viewed by others
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–524
Anthony KRN (2000) Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia). Coral Reefs 19:59–67
Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Bio Ecol 252:221–253
Aronson RB, Precht WF (1995) Landscape patterns of reef coral diversity: a test of the intermediate disturbance hypothesis. J Exp Mar Bio Ecol 192:1–14
Baars MA, Sumoto AB, Oosterhuis SS, Arinardi OH (1990) Zooplankton abundance in the eastern Banda Sea and northern Arafura Sea during and after the upwellings season, August 1984 and February 1985. Netherlands Journal of Sea Research 25:527–543
Barnes-Mauthe M, Oleson KLL, Zafindrasilivonona B (2013) The total economic value of small-scale fisheries with a characterization of post-landing trends: an application in Madagascar with global relevance. Fish Res 147:175–185
Bayer FM (1961) The shallow-water Octocorallia of the West Indian region. Martinus Nijhoff, The Hague
Bayer FM (1981) Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnoses of new taxa. Proceedings of the Biological Society of Washington 94:901–947
Bell JJ, Smith DJ (2004) Ecology of sponge assemblages (Porifera) in the Wakatobi region, south-east Sulawesi, Indonesia: richness and abundance. J Mar Biol Assoc UK 84:581–589
Benbow S, Humber F, Oliver TA, Oleson KL, Raberinary D, Nadon M, Ratsimbazafy H, Harris A (2014) Lessons learnt from experimental temporary octopus fishing closures in south-west Madagascar: benefits of concurrent closures. African Journal of Marine Science 36:31–37
Bohn K, Pavlick R, Reu B, Kleidon A (2014) The strengths of r- and K-selection shape diversity–disturbance relationships. PLoS One 9:e95659
Bramanti L, Magagnini G, De Maio L, Santangelo G (2005) Recruitment, early survival and growth of the Mediterranean red coral Corallium rubrum (L 1758), a 4-year study. J Exp Mar Bio Ecol 314:69–78
Bramanti L, Vielmini I, Rossi S, Tsounis G, Iannelli M, Cattaneo-Vietti R, Priori C, Santangelo G (2014) Demographic parameters of two populations of red coral (Corallium rubrum L. 1758) in the north-western Mediterranean. Mar Biol 161:1015–1026
Brazeau DA, Harvell CD (1994) Genetic structure of local populations and divergence between growth forms in a clonal invertebrate, the Caribbean octocoral Briareum asbestinum. Mar Biol 119:53–60
Buhl-Mortensen L, Vanreusel A, Gooday AJ, Levin LA, Priede IG, Buhl-Mortensen P, Gheerardyn H, King NJ, Raes M (2010) Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar Ecol 31:21–50
Buzas MA, Collins LS, Culver SJ (2002) Latitudinal difference in biodiversity caused by higher tropical rate of increase. Proc Natl Acad Sci U S A 99:7841–7843
Carpenter KE, Barber PH, Crandall ED, Ablan-Lagman MCA, Ambariyanto Mahardika GN, Manjaji-Matsumoto BM, Juinio-Meñez MA, Santos MD, Starger CJ, Toha AHA (2011) Comparative phylogeography of the Coral Triangle and implications for marine management. J Mar Biol 2011:396982
Cerrano C, Danovaro R, Gambi C, Pusceddu A, Riva A, Schiaparelli S (2010) Gold coral (Savalia savaglia) and gorgonian forests enhance benthic biodiversity and ecosystem functioning in the mesophotic zone. Biodivers Conserv 19:153–167
Chanmethakul T, Chansang H, Watanasit S (2010) Soft coral (Cnidaria: Alcyonacea) distribution patterns in Thai waters. Zool Stud 49:72–84
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143
Clarke KR, Gorley RN (2006) PRIMER v6: User manual/tutorial, 2nd edn. PRIMER-E Ltd, Plymouth, UK
Clarke KR, Somerfield PJ, Chapman MG (2006a) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. J Exp Mar Bio Ecol 330:55–80
Clarke KR, Chapman MG, Somerfield PJ, Needham HR (2006b) Dispersion-based weighting of species counts in assemblage analyses. Mar Ecol Prog Ser 320:11–27
Clifton J (2003) Prospects for co-management in Indonesia’s marine protected areas. Mar Policy 27:389–395
Clifton J (2013) Refocusing conservation through a cultural lens: improving governance in the Wakatobi National Park, Indonesia. Mar Policy 41:80–86
CoBabe EA, Allmon WD (1994) Effects of sampling on paleoecologic and taphonomic analyses in high-diversity fossil accumulations: an example from the Eocene Gosport Sand, Alabama. Lethaia 27:167–178
Coffroth MA, Lasker HR (1998) Population structure of a clonal gorgonian coral: the interplay between clonal reproduction and disturbance. Evolution 52:379–393
Connell JH (1978) Diversity in tropical forest and coral reefs. Science 199:1302–1310
Crabbe JC, Smith DJ (2003) Computer modeling and estimation of recruitment patterns of non-branching coral colonies at three sites in the Wakatobi Marine Park, S.E. Sulawesi, Indonesia; implications for coral reef conservation. Comput Biol Chem 27:17–27
Dauget J-M (1992) Effets d’un changement d’orientation de la colonie sure la morphologie de Isis hippuris Linne, 1758 (Gorgonacea): note preliminaire. Bulletin de la Société Zoologique de France 117:375–382
English SA, Wilkinson C, Baker VJ (1997) Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, Australia, p 390
Etnoyer PJ, Wirshing HH, Sánchez JA (2010) Rapid assessment of octocoral diversity and habitat on Saba Bank, Netherlands Antilles. PLoS One 5:e10668
Etnoyer PJ, Wickes LN, Silva M, Dubick JD, Balthis L, Salgado E, MacDonald IR (2016) Decline in condition of gorgonian octocorals on mesophotic reefs in the northern Gulf of Mexico: before and after the Deepwater Horizon oil spill. Coral Reefs 35:77–90
Exton DA (2010) Nearshore fisheries of the Wakatobi. In: Clifton J, Unsworth RKF, Smith DJ (eds) Marine research and conservation in the Coral Triangle: the Wakatobi National Park. Nova Science Publishers, Hauppauge, NY, pp 193–207
Fabricius KE, Klumpp DW (1995) Widespread mixotrophy in reef-inhabiting soft corals: the influence of depth, and colony expansion and contraction on photosynthesis. Mar Ecol Prog Ser 125:195–204
Fabricius KE, Alderslade P (2001) Soft corals and sea fans: a comprehensive guide to the tropical shallow-water general of the central-west Pacific, the Indian Ocean and the Red Sea. Australian Institute of Marine Science, Townsville, p 264
Fabricius KE, De’ath G (2004) Identifying ecological change and its causes: a case study on coral reefs. Ecol Appl 14:1448–1465
Fabricius KE, Alderslade P, Williams GC, Colin PL, Golbuu Y (2007) Octocorallia in Palau, Micronesia: effects of biogeography and coastal influences on local and regional biodiversity. In: Kayanne H, Omori M, Fabricius K, Verheij E, Colin P, Golbuu Y, Yurihira H (eds) Coral reefs of Palau. Palau International Coral Reef Centre, Palau, pp 79–92
Fabricius KE, McCorry D (2006) Changes in octocoral communities and benthic cover along a water quality gradient in the reefs of Hong Kong. Mar Pollut Bull 52:22–33
Fleury B, Coll J, Sammarco P (2006) Complementary (secondary) metabolites in a soft coral: sex-specific variability, inter-clonal variability, and competition. Mar Ecol 27:204–218
Garrabou J, Perez T, Sartoretto S, Harmelin JG (2001) Mass mortality event in red coral Corallium rubrum populations in the Provence region (France, NW Mediterranean). Mar Ecol Prog Ser 217:263–272
Gieskes WWC, Kraay GW, Nontji A, Setiapermana D, Sutomo D (1988) Monsoonal alterations of a mixed and a layer structure in the phytoplankton of the euphotic zone of the Banda Sea (Indonesia); a mathematical analysis of algal pigment fingerprints. Netherlands Journal of Sea Research 22:123–137
Goatley CHR, Bellwood DR (2011) The roles of dimensionality, canopies and complexity in ecosystem monitoring. PLoS One 6:e27307
Goh NKC, Chou LM (1994) Distribution and biodiversity of Singapore gorgonians (sub-class Octocorallia)—a preliminary survey. Hydrobiologia 285:101–109
Goldberg WM (1973) The ecology of the coral–octocoral communities off the southeast Florida coast: geomorphology, species composition, and zonation. Bull Mar Sci 23:465–488
Grasshoff M (1999) The shallow water gorgonians of New Caledonia and adjacent islands (Coelenterata: Octocorallia). Senckenb Biol 78:1–245
Grasshoff M (2001) Taxonomy, systematics, and octocorals: to Frederick M. Bayer, October 31st 2001. Bulletin of the Biological Society of Washington 10:3–14
Haapkylä J, Seymour AS, Trebilco J, Smith DJ (2007) Coral disease prevalence and coral health in the Wakatobi Marine National Park, south-east Sulawesi, Indonesia. J Mar Biol Ass UK 87:403–414
Hay ME (1986) Associational plant defenses and the maintenance of species diversity: turning competitors into accomplices. Am Nat 128:617–641
Hennige SJ, Smith DJ, Perkins R, Consalvey M, Paterson DD, Suggett DJ (2008) Photoacclimation, growth and distribution of massive coral species in clear and turbid waters. Mar Ecol Prog Ser 369:77–88
Hodgson A (2008) Spatial variation in reef echinoid abundance and diversity with habitat, fish community structure and anthropogenic pressure. Bachelors dissertation, Newcastle University, UK
Kingsford M, Battershill C (1998) Studying temperate marine environments: a handbook for ecologists. Canterbury University Press, New Zealand
Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216
Lenz EA, Bramanti L, Lasker HR, Edmunds PJ (2015) Long-term variation of octocoral populations in St. John, US Virgin Islands. Coral Reefs 34:1099–1109
Linares C, Coma R, Zabala M (2008a) Restoration of threatened red gorgonian populations: an experimental and modelling approach. Biol Conserv 141:427–437
Linares C, Coma R, Garrabou J, Díaz D, Zabala M (2008b) Size distribution, density and disturbance in two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J Appl Ecol 45:688–699
Matsumoto AK, Iwase F, Imahara Y, Namikawa H (2007) Bathymetric distribution and biodiversity of cold-water octocorals (Coelenterata: Octocorallia) in Sagami Bay and adjacent waters of Japan. Bull Mar Sci 81:231–252
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297
McCormick MI (1994) Comparison of field methods for measuring surface topography and their associations with a tropical reef fish assemblage. Mar Ecol Prog Ser 112:87–96
McFadden CS, Brown AS, Brayton C, Hunt CB, van Ofwegen LP (2014) Application of DNA barcoding in biodiversity studies of shallow-water octocorals: molecular proxies agree with morphological estimates of species richness in Palau. Coral Reefs 33:275–286
McLean EL, Yoshioka PM (2007) Associations and interactions between gorgonians and sponges. In: Custodio MR, Lobo-Hadju G, Hadju E, Muricy E (eds) Porifera research: biodiversity, innovation and sustainability. Museu Nacional, Rio de Janeiro, pp 443–448
McManus JW (1997) Tropical marine fisheries and the future of coral reefs: a brief review with emphasis on Southeast Asia. Coral Reefs 16:S121–S127
Nagib Edrus I, Suman A (2013) Policy synthesis on protection and conservation for octocorallian fauna (Isis hippuris Linnaeus 1758). Jurnal Kebijakan Perikanan Indonesia 5:107–112
Nutting CC (1910a) The Gorgonacea of the Siboga Expedition III. The Muriceidae. Siboga-Expeditie Monographie XIII, Brill, Leiden, The Netherlands, p 108
Nutting CC (1910b) The Gorgonacea of the Siboga Expedition IV. The Plexauridae. Siboga-Expeditie Monographie Monographie XIII, Brill, Leiden, The Netherlands, p 20
Nutting CC (1910c) The Gorgonacea of the Siboga Expedition V. The Isidae. Siboga- Expeditie Monographie XIII,, Brill, Leiden, The Netherlands, p 24
Nutting CC (1910d) The Gorgonacea of the Siboga Expedition VI. The Gorgonellidae. Siboga-Expeditie Monographie XIII, Brill, Leiden, The Netherlands, p 39
Nutting CC (1910e) The Gorgonacea of the Siboga Expedition VII. The Gorgoniidae. Siboga-Expeditie Monographie Monographie XIII, Brill, Leiden, The Netherlands, p 10
Nutting CC (1911) The Gorgonacea of the Siboga Expedition VIII. The Scleraxonia. Siboga-Expeditie Monographie Monographie XIII, Brill, Leiden, The Netherlands, p 62
Oliver TA, Oleson KL, Ratsimbazafy H, Raberinary D, Benbow S, Harris A (2015) Positive catch and economic benefits of periodic octopus fishery closures: do effective, narrowly targeted actions ‘catalyze’ broader management? PLoS One 10:e0129075
Paulay G, Puglisi MP, Starmer JA (2003) The non-scleractinian Anthozoa (Cnidaria) of the Mariana Islands. Micronesica 35–36:138–155
Peet RK (1974) The measurement of species diversity. Annu Rev Ecol Syst 5:285–307
Pilgrim SE, Cullen LC, Smith DJ, Pretty J (2007) Hidden harvest or hidden revenue? Local resource use in a remote region of Southeast Sulawesi, Indonesia. Indian Journal of Traditional Knowledge 6:150–159
Prada C, Schizas NV, Yoshioka PM (2008) Phenotypic plasticity or speciation? A case of a clonal marine organism. BMC Evol Biol 8:47
Puglisi MP, Paul VJ, Biggs J, Slattery M (2002) Co-occurrence of chemical and structural defenses in the gorgonian corals of Guam. Mar Ecol Prog Ser 239:105–114
Reijnen BT, McFadden CS, Hermanlimianto YT, van Ofwegen LP (2014) A molecular and morphological exploration of the generic boundaries in the family Melithaeidae (Coelenterata: Octocorallia) and its taxonomic consequences. Mol Phylogenet Evol 70:383–401
Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202
Rowley SJ (2014a) Gorgonian responses to environmental change on coral reefs in SE Sulawesi, Indonesia. PhD thesis, Victoria University of Wellington, New Zealand, p 213
Rowley SJ (2014b) Refugia in the ‘twilight zone’: discoveries from the Philippines. The Marine Biologist 2:16–17
Rowley SJ, Pochon X, Watling L (2015) Environmental influences on the Indo-Pacific octocoral Isis hippuris Linnaeus, 1758 (Alcyonacea: Isididae): genetic fixation or phenotypic plasticity? PeerJ 3:e1128
Samimi-Namin K, van Ofwegen LP, Wilson SC, Claereboudt MR (2011) The first in situ and shallow-water observation of the genus Pseudothelogorgia (Octocorallia: Keroeididae). Zool Stud 50:265
Sánchez JA (2004) Evolution and dynamics of branching colonial form in marine modular cnidarians: gorgonian octocorals. Hydrobiologia 530–531:283–290
Sánchez JA (2016) Diversity and evolution of octocoral animal forests at both sides of tropical America. In: Rossi S, Bramanti L, Gori A, Orejas C (eds) Marine animal forests. The ecology of benthic biodiversity hotspots, Springer International, pp 1–33
Sánchez JA, Diaz JM, Zea S (1997) Gorgonian communities in two contrasting environments on oceanic atolls of the southwest Caribbean. Bull Mar Sci 61:453–465
Sánchez JA, Zeng W, Coluci VR, Simpson C, Lasker HR (2003) How similar are branching networks in nature? A view from the ocean: Caribbean gorgonian corals. J Theor Biol 222:135–138
Sanciangco JC, Carpenter KE, Etnoyer PJ, Moretzsohn F (2013) Habitat availability and heterogeneity and the Indo-Pacific warm pool as predictors of marine species richness in the tropical Indo-Pacific. PLoS One 8:e56245
Scaps P, Denis V (2007) Association between the scallop, Pedum spondyloideum, (Bivalva: Pteriomorphia: Pectinidae) and scleractinian corals from the Wakatobi Marine National Park (southeastern Sulawesi, Indonesia). The Raffles Bulletin of Zoology 55:371–380
Sebens KP (1982) The limits to indeterminate growth: an optimal size model applied to passive suspension feeders. Ecology 63:209–222
Sebens KP (1984) Water flow and coral colony size: inter habitat comparisons of the octocoral Alcyonium siderium. Proc Natl Acad Sci U S A 81:5473–5477
Simpson JJ (1906) The structure of Isis hippuris, Linnaeus. Zool J Linn Soc 29:421–434
Stiasny G (1937) Die Gorgonacea der Siboga-Expedition. Suppl. II, Revision der Scleraxonia, etc. Siboga-Expeditie Monographie, Brill, Leiden, The Netherlands, p 133
Stiasny G (1940) Die Gorgonarien Sammlung der Snellius-Expedition. Temminckia 5:191–256
Tinsley P (2005) Worbarrow reefs seafan project 2003–2005. Dorset Wildlife Trust, http://www.seasearch.org.uk/downloads/Worbarrow%20Reefs%20Study.pdf
Tomascik T, Mah AJ, Nontji A, Kasim Moosa M (2004) The ecology of the Indonesian seas part one. Oxford University Press, p 642
Unsworth RK, Powell A, Hukom F, Smith DJ (2007) The ecology of Indo-Pacific grouper (Serranidae) species and the effects of a small scale no take area on grouper assemblage, abundance and size frequency distribution. Mar Biol 74:53–62
van Ofwegen LP (2004) The present status of taxonomic knowledge of octocorals in Indonesia. In: Tomascik T, Mah AJ, Nontji A, Kasim Moosa M (eds) The ecology of the Indonesian seas part one. Oxford University Press, Oxford, pp 345–346
Verseveldt J (1966) Biological results of the Snellius Expedition XXII. Octocorallia from the Malay Archipelago (Part II). Zoologische Verhandelingen Leiden 80:1–109
Versluys J (1902) Die Gorgoniden der Siboga-Expedition. I. Die Chrysogorgiiden, volume 13. Monographie Siboga-Expeditie, Brill, Leiden, The Netherlands, p 120
Versluys J (1906) Die Gorgoniden der Siboga Expedition II. Die Primnoidae. Siboga- Expeditie Monographie XIII, 178. pls. 1_10
von Heland F, Clifton J, Olsson P (2014) Improving stewardship of marine resources: linking strategy to opportunity. Sustainability 6:4470–4496
Wald A, Wolfowitz J (1943) An exact test for randomness in the non-parametric case based on serial correlation. Annals of Mathematical Statistics 14:378–388
Weiner J (2004) Allocation, plasticity and allometry in plants. Perspectives in Plant Ecology, Evolution and Systematics 6:207–215
Wentworth CK (1922) A scale of grade and class terms for clastic sediments. J Geol 30:377–392
West JM (1997) Plasticity in the sclerites of a gorgonian coral: tests of water motion, light level, and damage cues. Biol Bull 192:279–289
West JM, Harvell CD, Walls AM (1993) Morphological plasticity in a gorgonian coral (Briareum asbestinum) over a depth cline. Mar Ecol Prog Ser 94:61–69
Yoshioka PM, Yoshioka BB (1989) Effects of water motion, topographic relief and sediment transport on the distribution of shallow-water gorgonian community. Mar Ecol Prog Ser 54:257–264
Acknowledgements
This study was made possible by the generous support of the Wakatobi Government, the Indonesian staff at ALAM of the Wakatobi Marine National Park, and the Wallacea Foundation, particularly Pak Iwan, Arif and Azrul. The State Ministry of Research and Technology (RISTEK) granted research permits to Prof. D. J. Smith, under whose auspices this work was conducted. This manuscript benefited from spirited discussion and guidance from Profs. S. M. Stanley, S. K. Davy, J. Gardner, C. Birkeland, C. Todd, L. Watling, Drs. J. J. Bell, A. Rowden, R. L. Pyle and G. Williams, as well as insightful comments from two anonymous reviewers. S. J. R was supported by a Victoria University Wellington Doctoral Research Scholarship and the Coral Reef Research Unit, with sponsorship from P Duxfield at Cameras Underwater for camera equipment.
Author information
Authors and Affiliations
Corresponding author
Additional information
Topic Editor Dr. Alastair Harborne
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rowley, S.J. Environmental gradients structure gorgonian assemblages on coral reefs in SE Sulawesi, Indonesia. Coral Reefs 37, 609–630 (2018). https://doi.org/10.1007/s00338-018-1685-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-018-1685-y