Abstract
Sea urchins of the genus Diadema, key herbivores in coral reef ecosystems, also provide habitat for other organisms. Our research extended Diadema biogeography in seaways east and west of Sulawesi and identified Diadema species associated with the endemic Banggai cardinalfish (Pterapogon kauderni) using field surveys and molecular DNA barcoding methods. Field observations (20 sites, n = 11,223) found urchins with morphological phenotypes typical of Diadema setosum (≈ 74%, all sites), D. savignyi (≈ 24%, 19 sites) and atypical or mixed traits (≈ 2%, 19 sites). Distribution of these phenotype groups across the three main habitat types (i.e. coral reef, reef flat and seagrass beds) differed significantly (χ2 = 533.03, p < 2.2e−16), indicating overlapping but non-equivalent ecological niches. Pterapogon kauderni associated with all urchin morphological phenotypes present. Diadema mtDNA CO1 sequences were obtained from tissue samples collected (4 sites, n = 62) from specimens with typical D. savignyi and D. setosum phenotypes. Phylogenetic tree analysis resolved the sequences into four clades. Three clades from our analysis were identified as D. savignyi, D. setosum and D. clarki based on additional sequences obtained from GenBank. This unexpected first record of D. clarki mtDNA in the Coral Triangle implies a substantial extension of the known range of this recently resurrected species. Our findings indicate the occurrence and/or introgression of D. clarki may be widespread, and misidentification of Diadema urchins based on external morphology may be relatively common. Further research is required to determine the distribution and functional roles of Indo-Pacific Diadema species, contributing to our understanding of processes underpinning biodiversity.
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References
Addison JA, Kim JH (2018) Cryptic species diversity and reproductive isolation among sympatric lineages of Strongylocentrotus sea urchins in the northwest Atlantic. FACETS 3(1):61–78. https://doi.org/10.1139/facets-2017-0081facetsjournal.com
Agassiz A (1863) List of the echinoderms sent to different institutions in exchange for other specimens, with annotations. Bull Mus Comp Zool 1:17–28
Ahmadia GN, Tornabene L, Smith DJ, Pezold FL (2018) The relative importance of regional, local, and evolutionary factors structuring cryptobenthic coral-reef assemblages. Coral Reefs 37(1):279–293. https://doi.org/10.1007/s00338-018-1657-2
Allen GR (2008) Conservation hotspots of biodiversity and endemism for Indo-Pacific coral reef fishes. Aquat Conserv 18(5):541–556. https://doi.org/10.1002/aqc.880
Allen G R, Donaldson T J (2007) Pterapogon kauderni. The IUCN red list of threatened species 2007: e.T63572A12692964. https://doi.org/10.2305/IUCN.UK.2007.RLTS.T63572A12692964.en. Accessed 21 January 2019.
Al-Rshaidat MM, Snider A, Rosebraugh S, Devine AM, Devine TD, Plaisance L, Knowlton N, Leray M (2016) Deep COI sequencing of standardized benthic samples unveils overlooked diversity of Jordanian coral reefs in the northern Red Sea. Genome 59(9):724–737. https://doi.org/10.1139/gen-2015-0208
Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Syst Biol 55(4):539–552. https://doi.org/10.1080/10635150600755453
Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25(3):441–450. https://doi.org/10.1007/s00338-006-0122-9
Audouin, V (1809) Explication sommaire des planches d’Échinoderms de l’Égypte et de la Syrie, publiées par J. C. Savigny, membre de L’Institut; offrant un exposé des caractères naturels des genres avec la distinction des espèces. In: de Savigny J C (ed) Description de L’Égypte ou recueil des observations et des recherches qui ont été faites en Égypte pendant l’Expédition de l’Armée Française, publié par les ordres de sa majesté l'empereur Napoléon le Grand. Histoire Naturelle, Tome Premier, Quatrième Partie: Explication sommaire des planches dont les dessins ont été fournis par M. J. Savigny, pour l’histoire naturelle de l’ouvrage. L’Imprimerie Impériale, Paris, pp. 203–12
Barber PH (2009) The challenge of understanding the Coral Triangle biodiversity hotspot. J Biogeogr 36(10):1845–1846
Baker AN (1967) Two new echinoids from Northern New Zealand, including a new species of Diadema. Trans R Soc New Zeal 8(23)
Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22(3):147–155. https://doi.org/10.1016/j.tree.2006.11.004
Birkeland C (1989) The influence of echinoderms on coral-reef communities. In: Jangoux M, Lawrence JM (eds) Echinoderm studies, vol vol 3. AA Balkema, Rotterdam, 79pp
Bowen BW, Rocha LA, Toonen RJ, Karl SA (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28(6):359–366. https://doi.org/10.1016/j.tree.2013.01.018
Bribiesca-Contreras G, Solis-Marin FA, Laguarda-Figueras A, Zaldivar-Riveron A (2013) Identification of echinoderms (Echinodermata) from an anchialine cave in Cozumel Island, Mexico, using DNA barcodes. Mol Ecol Resour 13(6):1137–1145. https://doi.org/10.1111/1755-0998.12098
Bronstein O, Loya Y (2014) Echinoid community structure and rates of herbivory and bioerosion on exposed and sheltered reefs. J Exp Mar Biol Ecol 456:8–17. https://doi.org/10.1016/j.jembe.2014.03.003
Bronstein O, Kroh A, Haring E (2016) Do genes lie? Mitochondrial capture masks the Red Sea collector urchin’s true identity (Echinodermata: Echinoidea: Tripneustes). Mol Phylogenet Evol 104:1–13. https://doi.org/10.1016/j.ympev.2016.07.028
Bronstein O, Georgopoulou E, Kroh A (2017) On the distribution of the invasive long-spined echinoid Diadema setosum and its expansion in the Mediterranean Sea. Mar Ecol Prog Ser 583:163–178. https://doi.org/10.3354/meps12348
Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA barcoding of marine metazoa. Annu Rev Mar Sci 3:471–508. https://doi.org/10.1146/annurev-marine-120308-080950
Carpenter KI, Barber PH, Crandall ED, Ablan-Lagman CA, Ambariyanto, Mahardika GN, Manjaji-Matsumoto M, Juinio-Meñez MA, Santos MD, Starger CJ, Toha AHA (2011) Comparative phylogeography of the Coral Triangle and implications for marine management. J Mar Biol:396982. https://doi.org/10.1155/2011/396982
Carpenter RC, Edmunds PJ (2006) Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol Lett 9(3):268–277. https://doi.org/10.1111/j.1461-0248.2005.00866.x
Carreiro-Silva M, McClanahan TR (2001) Echinoid bioerosion and herbivory on Kenyan coral reefs: the role of protection from fishing. J Exp Mar Biol Ecol 262:133–153. https://doi.org/10.1016/S0022-0981(01)00288-X
Chow S, Kajigaya Y, Kurogi H, Niwa K, Shibuno T (2014) On the fourth Diadema species (Diadema-sp) from Japan. PLoS One 9(7):e102376. https://doi.org/10.1371/journal.pone.0102376
Chow S, Konish K, Mekuchi M, Tamaki Y, Nohara K, Takagi M, Niwa K, Teramoto W, Manabe H, Kurogi H, Suzuki S, Ando D, Jinbo T, Kiyomoto M, Hirose M, Shimomura M, Kurashima A, Ishikawa T, Kiyomoto S (2016) DNA barcoding and morphological analyses Echinoidea, Diadematidae. ZooKeys 585:1–16. https://doi.org/10.3897/zookeys.585.8161
Coppard SE, Campbell AC (2004) Organisms associated with diadematid echinoids in Fiji. In: Echinoderms: Munchen, Proc 11th International Echinoderm Conference, 6–10 October 2003, Munich, Germany 171–175
Coppard SE, Campbell AC (2005) Lunar periodicities of diadematid echinoids breeding in Fiji. Coral Reefs 24(2):324–332. https://doi.org/10.1007/s00338-005-0491-5
Coppard SE, Campbell AC (2007) Grazing preferences of diadematid echinoids in Fiji. Aquat Bot 86:204–212. https://doi.org/10.1016/j.aquabot.2006.10.005
Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17(2):611–626. https://doi.org/10.1111/j.1365-294X.2007.03600.x
Crandall ED, Treml EA, Barber PH (2012) Coalescent and biophysical models of stepping-stone gene flow in neritid snails. Mol Ecol 21(22):5579–5598. https://doi.org/10.1111/mec.12031
de Beer M (1990) Distribution patterns of regular sea urchins (Echinodermata: Echinoidea) across the Spermonde Shelf, SW Sulawesi (Indonesia). In: Ridder D, Lahaye J (eds) Echinoderm research. Balkema, Rotterdam, pp 165–169
Egea E, David B, Choné T, Laurin B, Féral JP, Chenuil A (2016) Morphological and genetic analyses reveal a cryptic species complex in the echinoid Echinocardium cordatum and rule out a stabilizing selection explanation. Mol Phylogenet Evol 94:207–220. https://doi.org/10.1016/j.ympev.2015.07.023
Erpenbeck D, Aryasari R, Benning S, Debitus C, Kaltenbacher E, Al-Aidaroos AM, Schupp P, Hall K, Hooper JN, Voigt O, de Voogd NJ (2017) Diversity of two widespread Indo-Pacific demosponge species revisited. Mar Biodivers 47(4):1035–1043. https://doi.org/10.1007/s12526-017-0783-3
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Geller J, Meyer C, Parker M, Hawk H (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Mol Ecol Resour 13(5):851–856. https://doi.org/10.1111/1755-0998.12138
Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7(4):457–472. https://doi.org/10.1214/ss/1177011136
Gray JE (1825) An attempt to divide the Echinida or sea-eggs into natural families. Ann Philos London 26:423–431
Grygier M J, Newman WA (1991) A new genus and two new species of Microlepadidae (Cirripedia: Pedunculata) found on Western Pacific Diadematid Echinoids, pp 1–22. In: Galaxea, volume 10. Sesoko Marine Science Center, University of the Ryukyus, Nishihara
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704. https://doi.org/10.1080/10635150390235520
Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174. https://doi.org/10.1007/BF02101694
Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1007/978-1-4020-6754-9_3188
Hoareau TB, Boissin E (2010) Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata. Mol Ecol Resour 10(6):960–967. https://doi.org/10.1111/j.1755-0998.2010.02848.x
Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S (2017) Coral reef ecosystems under climate change and ocean acidification. Front Mar Sci 4:158. https://doi.org/10.3389/fmars.2017.00158
Hoffman EA, Kolm N, Berglund A, Arguello JR, Jones AG (2005) Genetic structure in the coral-reef-associated Banggai cardinalfish, Pterapogon kauderni. Mol Ecol 14:1367–1375. https://doi.org/10.1111/j.1365-294X.2005.02538.x
Holland BS, Dawson MN, Crow GL, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145(6):1119–1128. https://doi.org/10.1007/s00227-004-1409-4
Huelsken T, Keyse J, Liggins L, Penny S, Treml EA, Riginos C (2013) A novel widespread cryptic species and phylogeographic patterns within several giant clam species (Cardiidae: Tridacna) from the Indo-Pacific Ocean. PLoS One 8(11):e80858. https://doi.org/10.1007/s00227-004-1409-4
iBOL (2010) Diadema antillarum voucher BIOUG<CAN>:BAHA-019 cytochrome oxidase subunit 1 (COI) gene, partial. International Barcode of Life (iBOL). Direct submission. https://www.ncbi.nlm.nih.gov/nuccore/296831796
Ikeda H (1939) A new species of Diadema from Japan. Records of Oceanographic Works in Japan, vol 10, Tokyo Science Council of Japan, pp 165–167
Imajima M, Hove HAT (1984) Serpulinae (Annelida, Polychaeta) from the Truk Islands, Ponape and Majuro Atoll, with some other new Indo-Pacific records. Proc Jap Soc Syst Zool 27:35–66. https://doi.org/10.19004/pjssz.27.0_35
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/s00227-004-1409-4
Kolm N, Berglund A (2003) Wild populations of a reef fish suffer from the “non-destructive” aquarium trade fishery. Conserv Biol 17(3):910–914. https://doi.org/10.1046/j.1523-1739.2003.01522.x
Koumans FP (1933) On a new genus and species of Apogonidae. Zool Melded 6(1–2):78 pl.1
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Ladner JT, Palumbi SR (2012) Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes. Mol Ecol 21(9):2224–2238. https://doi.org/10.1111/j.1365-294X.2012.05528.x
Lawrence JM (ed) (2006) Edible sea urchins: biology and ecology. Elsevier, Amsterdam
Lawrence JM (ed) (2013) Sea urchins: biology and ecology, 3rd edn. Elsevier, Amsterdam
Lee S-Y, Huh C-A, Su C-C, You C-F (2004) Sedimentation in the Southern Okinawa Trough: enhanced particle scavenging and teleconnection between the Equatorial Pacific and western Pacific margins. Deep-Sea Res I 51:1769–1780. https://doi.org/10.1016/j.dsr.2004.07.008
Lee T (2011) A systematic study of Korean echinoids based on morphology and molecular phylogeny. Thesis, Sahmyook University, Seoul, South Korea. 92pp
Leske N G (1778) Jacobi Theodori Klein Naturalis dispositio echinodermatum. Accesserunt Lucubratiuncula de aculeis echinorum marinorum et Spicilegium de belemnitis. Edita et descriptionibus novisque inventis et synonymis auctorum aucta a Nathanaele Godofredo Lesk cum 54 tabulis aeneis. G. E. Beer, Leipzig, xxii+278 pp
Lessios HA (2007) Reproductive isolation between species of sea urchins. Bull Mar Sci 81(2):191–208 https://www.ingentaconnect.com/content/umrsmas/bullmar/2007/00000081/00000002/art00007
Lessios HA (2016) The great Diadema antillarum die-off: 30 years later. Annu Rev Mar Sci 8(1):267–283. https://doi.org/10.1146/annurev-marine-122414-033857
Lessios HA, Pearse JS (1996) Hybridization and introgression between Indo-Pacific species of Diadema. Mar Biol 126(4):715–723. https://doi.org/10.1007/BF00351338
Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55(5):955–975. https://doi.org/10.1554/0014-3820(2001)055[0955:PSASIT]2.0.CO;2
Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. https://doi.org/10.1093/nar/gkz239
Li C, Wu G, Fu W, Zeng X (2016) The complete mitochondrial genome of Diadema setosum (Aulodonta: Diadematidae). Mitochondrial DNA B Resour 1(1):873–874. https://doi.org/10.1080/23802359.2016.1253039
Lilley R (2008) The Banggai cardinalfish: an overview of conservation challenges. SPC Live Reef Fish Inf Bull 18:3–12 http://www.spc.int/DigitalLibrary/Doc/FAME/InfoBull/LRF/18/LRF18_03_Lilley.pdf
Lunn KE, Moreau MA (2004) Unmonitored trade in marine ornamental fishes: the case of Indonesia’s Banggai cardinalfish (Pterapogon kauderni). Coral Reefs 23(3):344–351. https://doi.org/10.1007/s00338-004-0393-y
Maciá S, Robinson MP, Nalevanko A (2007) Experimental dispersal of recovering Diadema antillarum increases grazing intensity and reduces macroalgal abundance on a coral reef. Mar Ecol Prog Ser 348:173–182. https://doi.org/10.3354/meps06962
Magnus D B E (1967) Ecological and ethological studies and experiments on the echinoderms of the Red Sea. In: Proceedings of the International Conference on Tropical Oceanography 1965. Studies in Tropical Oceanography Issue5, University of Miami, Miami, pp 635–664
Mah CL, Blake DB (2012) Global diversity and phylogeny of the Asteroidea (Echinodermata). PLoS One 7(4):e35644. https://doi.org/10.1371/journal.pone.0035644
McClanahan TR (1988) Coexistence in a sea urchin guild and its implications to coral reef diversity and degradation. Oecologia 77(2):210–218. https://doi.org/10.1007/BF00379188
Miller MJ, Otake T, Minagawa G, Inagaki T, Tsukamoto K (2002) Distribution of leptocephali in the Kuroshio Current and East China Sea. Mar Ecol Prog Ser 235:279–288. https://doi.org/10.3354/meps235279
Milne I, Wright F, Rowe G, Marshal DF, Husmeier D, McGuire G (2004) TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20(11):1806–1807. https://doi.org/10.1093/bioinformatics/btn575
Moore A, Ndobe S (2007) Discovery of an introduced Banggai cardinalfish population in Palu Bay, Central Sulawesi, Indonesia. Coral Reefs 26:569. https://doi.org/10.1007/s00338-007-0227-9
Moore A, Ndobe S, Salanggon AIM, Ederyan A, Rahman A (2012) Banggai cardinalfish ornamental fishery: the importance of microhabitat. Proc 12th Int Coral Reef Symp 13C 1:1–5. http://www.icrs2012.com/proceedings/manuscripts/ICRS2012_13C_1.pdf
Moore A, Ndobe S, Jompa J (2017a) A site-based conservation approach to promote the recovery of Banggai cardinalfish (Pterapogon kauderni) endemic populations. Coast Ocean J 1(2):63–72. http://coj.pksplipb.or.id/index.php/coj/article/view/44/8
Moore A, Ndobe S, Jompa J (2017b) Fingerprints of the Anthropocene: the 2016 coral bleaching event in an equatorial archipelago. In Proc 4th International Marine and Fisheries Symposium, Hasanuddin University, Makassar, pp 66–86. https://doi.org/10.31230/osf.io/q5frc
Moore AM, Ndobe S, Yasir I, Ambo-Rappe R, Jompa J (2019) Banggai cardinalfish and its microhabitats in a warming world: a preliminary study. IOP Conf Ser: Earth Environ Sci 253:012021. https://doi.org/10.1088/1755-1315/253/1/012021
Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375. https://doi.org/10.1016/j.jembe.2009.04.004
Mortensen T (1940) A monograph of the Echinoidea, volume 3: Aulodonta 1. CA Reitzel, Copenhagen, 370 pp
Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101. https://doi.org/10.1038/nature06252
Muthiga NA (2003) Coexistence and reproductive isolation of the sympatric echinoids Diadema savignyi Michelin and Diadema setosum (Leske) on Kenyan coral reefs. Mar Biol 143(4):669–677. https://doi.org/10.1007/s00227-003-1095-7
Ndobe S, Setyohadi D, Herawati EY, Soemarno MA, Palomares MD, Pauly D (2013a) Life history of Banggai cardinalfish (Pterapogon kauderni; Pisces, Apogonidae) in Banggai Islands and Palu Bay, Sulawesi, Indonesia. Acta Ichthyol Piscat 43(3):237–250. https://doi.org/10.3750/AIP2013.43.3.08
Ndobe S, Moore A, Salanggon AIM, Muslihuddin, Setyohadi D, Herawati EY, Soemarno (2013b) Banggai cardinalfish (Pterapogon kauderni) management: an ecosystem-based approach. Mar Fish 4(2):115–126. https://doi.org/10.29244/jmf.4.2.115-126
Ndobe S, Moore A, Jompa J (2017) Status of and threats to microhabitats of the endangered endemic Banggai cardinalfish (Pterapogon kauderni). Coast Ocean J 1(2):73–82. http://coj.pksplipb.or.id/index.php/coj/article/view/45/9
Ndobe S, Yasir I, Moore A M, Biondo MV, Foster SJ (2018a) A study to assess the impact of international trade on the conservation status of Pterapogon kauderni (Banggai cardinalfish). https://cites.org/sites/default/files/eng/com/ac/30/Inf/E-AC30-Inf-16.pdf. Accessed 13 July 2018
Ndobe S, Jompa J, Moore A (2018b) A tale of two urchins – implications for in-situ breeding of the endangered Banggai cardinalfish (Pterapogon kauderni). Aquacultura Indonesiana 19(2):65–75. https://doi.org/10.21534/ai.v19i2.110
Ndobe S, Moore A, Yasir I, Jompa J (2019) Banggai cardinalfish conservation: priorities, opportunities, and risks. IOP Conf Ser: Earth Environ Sci 253:012033. https://doi.org/10.1088/1755-1315/253/1/012033
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Anu Rev Ecol Syst 25:547–572. https://doi.org/10.1146/annurev.es.25.110194.002555
Paz-García DA, Valencia-Méndez O, Domínguez-Domínguez O, Balart EF (2016) Living on the edge: Diadema mexicanum in the upper Gulf of California. Mar Biodivers 48(2):1261–1264. https://doi.org/10.1007/s12526-016-0539-5
Pearse JS (1990) Lunar reproductive rhythms in marine invertebrates: maximizing fertilization? In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction 5. Elsevier Science Publishers, Amsterdam, pp 311–322
Pearse JS (1998) Distribution of Diadema savignyi and D. setosum in the tropical Pacific. In: Echinoderms: San Francisco. AA Balkema, Rotterdam, pp 777–782
Philippi RA (1845) Beschreibung einiger neuer Echinodermen nebst kritischen Bemerckungen über einige weniger bekannte Arten. Archiv für Naturgeschichte 11:44–359
Pittauer D, Tims SG, Froehlich MB, Fifield LK, Wallner A, Mcneil SD, Fischer HW (2017) Continuous transport of Pacific-derived anthropogenic radionuclides towards the Indian Ocean. Sci Rep 7(44679):1–8. https://doi.org/10.1038/srep44679
Ponder WF, Gooding RU (1978) Four new eulimid gastropods associated with shallow-water diadematid echinoids in the western Pacific. Pacific Science volume 32, number 2. University of Hawaii Press, pp 157–181. http://hdl.handle.net/10125/1429
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/
Rodriguez A, Hernández JC, Clemente S, Coppard SE (2013) A new species of Diadema (Echinodermata: Echinoidea: Diadematidae) from the eastern Atlantic Ocean and a neotype designation of Diadema antillarum (Philippi, 1845). Zootaxa 636(1):144–170. https://doi.org/10.11646/zootaxa.3636.1.6
Rogers A, Lorenzen K (2016) Does slow and variable recovery of Diadema antillarum on Caribbean fore-reefs reflect density dependent habitat selection? Front Mar Sci 3(63):1–10. https://doi.org/10.3389/fmars.2016.00063
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. https://doi.org/10.1093/bioinformatics/btg180
R Studio Team (2016) RStudio: integrated development for R. RStudio, Inc., Boston http://www.rstudio.com/
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Stöhr S, O’Hara TD, Thuy B (2012) Global diversity of brittle stars (Echinodermata: Ophiuroidea). PLoS One 7(3):e31940. https://doi.org/10.1371/journal.pone.0031940
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighborjoining method. Proc Natl Acad Sci 101:11030–11035. https://doi.org/10.1073/pnas.0404206101
Tornabene L, Ahmadia GN, Berumen ML, Smith DJ, Jompa J, Pezold F (2013) Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: Gobiidae: Eviota). Mol Phylogenet Evol 66:391–400. https://doi.org/10.1016/j.ympev.2012.10.014
Uehara T, Asakura H, Arakaki Y (1990) Fertilization flockage and hybridization among species of sea urchins. In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction 5. Elsevier Science Publishers, Amsterdam, pp 305–310
Unsworth RKF, Ambo-Rappe R, Jones BL, La Nafie YA, Irawan A, Hernawan UE, Moore AM, Cullen-Unsworth LC (2018) Indonesia’s globally significant seagrass meadows are under widespread threat. Sci Total Environ 634:279–286. https://doi.org/10.1016/j.scitotenv.2018.03.315
Uthicke S, Byrne M, Conand C (2010) Genetic barcoding of commercial Beche-de-mer species (Echinodermata: Holothuroidea). Mol Ecol Resour 10(4):634–646. https://doi.org/10.1111/j.1755-0998.2009.02826.x
Vagelli A, Burford M, Bernardi G (2009) Fine scale dispersal in Banggai cardinal fish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Mar Genomics 1(3–4):129–134. https://doi.org/10.1016/j.margen.2009.01.001
Vagelli AA (2011) The Banggai cardinalfish: natural history, conservation, and culture of Pterapogon kauderni. John Wiley & Sons, Ltd, Chichester
Veron JEN, Devantier LM, Turak E, Green AL, Kininmonth S, Stafford-Smith M, Peterson N (2009) Delineating the Coral Triangle. Galaxea 11(2):91–100. https://doi.org/10.3755/galaxea.11.91
Victor BC (2015) How many coral reef fish species are there? Cryptic diversity and the new molecular taxonomy. In: Mora C (ed) Ecology of fishes on coral reefs. Cambridge University Press, Cambridge, pp 23–76
von der Heyden S, Beger M, Toonen RJ, van Herwerden L, Juinio-Meñez MA, Ravago-Gotanco R, Fauvelot C, Bernardi G (2014) The application of genetics to marine management and conservation: examples from the Indo-Pacific. Bull Mar Sci 90(1):123–158. https://doi.org/10.5343/bms.2012.1079
Watanabe S, Aoyama J, Tsukamoto K (2009) A new species of freshwater eel Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fish Sci 75:387–392. https://doi.org/10.1007/s12562-009-0087-z
Willette DA, Allendorf FW, Barber PH, Barshis DJ, Carpenter KE, Crandall ED, Cresko WA, Fernandez-Silva I, Matz MV, Meyer E, Santos MD, Seeb LW, Seeb JE (2014) So, you want to use next generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute. Bull Mar Sci 90(1):79–122. https://doi.org/10.5343/bms.2013.1008
Wilson CC, Bernatchez L (1998) The ghost of hybrids past: fixation of arctic charr (Salvelinus alpinus) mitochondrial DNA in an introgressed population of lake trout (S. namaycush). Mol Ecol 7(1):127–132. https://doi.org/10.1046/j.1365-294x.1998.00302.x
Acknowledgements
The authors wish to thank the many organisations and individuals who assisted with or facilitated the research and the production of this manuscript, including the BIONESIA team (molecular biology laboratory) and Muh. Banda Selamat (assistance with Fig. 1). We also wish to express our sincere gratitude to the three reviewers for their contributions which have enriched and improved the manuscript, to our editor for her unflagging support and patience and to all the Marine Biodiversity editorial team.
Funding
This study was funded by grant 3663/UN4.21/LK.23/2017 from the Hasanuddin University Professorship scheme, grant 3083/UN4.21/PL.00.00/2018 from the Hasanuddin University International Research Collaboration and Scientific Publication scheme and grant No. 168.A8/D2/KP/2017 from the Indonesian Ministry of Research, Technology, and Higher Education World Class Professor Scheme B. Preparation of the manuscript was supported by World Class Professor Scheme B Grant No. 168.A8/D2/KP/2017 from the Indonesian Ministry of Research, Technology, and Higher Education.
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All applicable international, national and/or institutional guidelines for the care and use of animals were followed by the authors.
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All necessary permitting and procedures were followed for the observational field study and the collection of samples, and the appropriate documents were provided to and/or obtained by the authors from the competent authorities.
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The datasets generated during the current study have been deposited in the GenBank repository under MG988406–MG988411, MH051847–MH051888 and MK296413–MK296426.
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Moore, A.M., Tassakka, A.C.M., Ambo-Rappe, R. et al. Unexpected discovery of Diadema clarki in the Coral Triangle. Mar Biodiv 49, 2381–2399 (2019). https://doi.org/10.1007/s12526-019-00978-4
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DOI: https://doi.org/10.1007/s12526-019-00978-4