Abstract
Nanipora Miyazaki & Reimer, 2015 is a recently described monotypic octocoral genus belonging to the family Helioporidae (class Octocorallia). Nanipora kamurai Miyazaki & Reimer, 2015 was formally described from shallow coral reefs around Zamami Island, within Kerama-shoto National Park, in Okinawa Prefecture, southern Japan. To date, Nanipora has been reported from two other locations in Japan: N. aff. kamurai from a shallow inner lagoon at Iriomotejima Island, and Nanipora cf. kamurai from the coral reef surrounding a shallow CO2 vent at Iotorishima Island, both in Okinawa Prefecture. Additionally, Nanipora cf. kamurai has been reported from three locations outside Japan: in shallow seagrass meadows at Dongsha Atoll in the South China Sea, on coral reefs at Koh Tao in Thailand and from a reef in Toboso, central Philippines. Finally, N. kamurai has been detected in environmental DNA samples from the Rowley Shoals off northwestern Australia. As a ‘living fossil’ and also apparently common in the low pH environment of Iotorishima I., a clearer understanding of the distribution of the genus should aid in better understanding of its ecology. Here, we report three new additional records from the Ryukyu Archipelago where Nanipora colonies were found, resulting in ten total records of Nanipora. Molecular phylogenetic analyses utilizing cytochrome oxidase subunit I (COI), mitochondrial mismatch repair protein (mtMutS), and the internal transcribed spacer region (ITS) sequences of specimens from two of these new locations combined with additional sequences from previously collected specimens from Dongsha, Iotorishima, and Iriomotejima showed evidence of three closely related groups within Nanipora, warranting future investigations into the species diversity of this genus.
This is a preview of subscription content, log in via an institution to check access.
Source: Esri Satellite. ArcGIS® ‘World_Imagery’
Similar content being viewed by others
References
Arrigoni R, Kitano YF, Stolarski J, Hoeksema BW, Fukami H, Stefani F, Galli P, Montano S, Castoldi E, Benzoni F (2014) A phylogeny reconstruction of the Dendrophylliidae (Cnidaria, Scleractinia) based on molecular and micromorphological criteria, and its ecological implications. Zool Scr 43:661–688. https://doi.org/10.1111/zsc.12072
Bayer FM, Muzik KM (1977) An Atlantic helioporan coral (Coelenterata: Octocorallia). Proc Biol Soc Wash 90:975–984
DiBattista J, Reimer JD, Stat M, Masucci G, Biondi P, De Brauwer M, ... Bunce M (2020) Environmental DNA can act as a biodiversity barometer of anthropogenic pressures in coastal ecosystems. Sci Rep 10:8365. https://doi.org/10.1038/s41598-020-64858-9
Dugal L, Thomas L, Wilkinson SP, Richards ZT, Alexander JB, Adam AA, Kennington WJ, Jarman S, Ryan NM, Bunce M, Gilmour JP (2022) Coral monitoring in northwest Australia with environmental DNA metabarcoding using a curated reference database for optimized detection. Environ DNA 4:63–76. https://doi.org/10.1002/edn3.199
France SC, Hoover LL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471:149–155. https://doi.org/10.1023/A:1016517724749
Guzman C, Atrigenio M, Shinzato C, Aliño P, Conaco C (2019) Warm seawater temperature promotes substrate colonization by the blue coral, Heliopora coerulea. PeerJ 7:e7785. https://doi.org/10.7717/peerj.7785
Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24. https://doi.org/10.1186/1471-2148-6-24
Hoeksema BW, Best MB (1991) New observations on scleractinian corals from Indonesia: 2. Sipunculan-associated species belonging to the genera Heterocyathus and Heteropsammia. Zool Meded 65:221–245
Kawahata H, Ohta H, Inoue M, Suzuki A (2004) Endocrine disrupter nonylphenol and bisphenol A contamination in Okinawa and Ishigaki Islands, Japan—within coral reefs and adjacent river mouths. Chemosphere 55:1519–1527. https://doi.org/10.1016/j.chemosphere.2004.01.032
Kayanne H, Harii S, Ide Y, Akimoto F (2002) Recovery of coral populations after the 1998 bleaching on Shiraho Reef, in the southern Ryukyus, NW Pacific. Mar Ecol Prog Ser 239:93–103. https://www.int-res.com/abstracts/meps/v239/p93-103/
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580. https://doi.org/10.1016/j.cub.2018.07.008
McFadden CS, Tullis ID, Hutchinson MB, Winner K, Sohm JA (2004) Variation in coding (NADH dehydrogenase subunits 2, 3, and 6) and noncoding intergenic spacer regions of the mitochondrial genome in Octocorallia (Cnidaria: Anthozoa). Mar Biotechnol 6:516–526. https://doi.org/10.1007/s10126-002-0102-1
McFadden CS, France SC, Sánchez JA, Alderslade P (2006) A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol Phylogenet Evol 41(3):513–527. https://doi.org/10.1016/j.ympev.2006.06.010
McFadden CS, Sánchez JA, France SC (2010) Molecular phylogenetic insights into the evolution of Octocorallia: A review. Integr Comp Biol 50:389–410. https://doi.org/10.1093/icb/icq056
McFadden CS, Benayahu Y, Pante E, Thoma JN, Nevarez PA, France SC (2011) Limitations of mitochondrial gene barcoding in Octocorallia. Mol Ecol Resour 11:19–31. https://doi.org/10.1111/j.1755-0998.2010.02875.x
McFadden CS, Van Ofwegen LP, Quattrini AM (2022) Revisionary systematics of Octocorallia (Cnidaria: Anthozoa) guided by phylogenomics. BSSB 1. https://doi.org/10.18061/bssb.v1i3.8735
McFadden CS, Cordeiro R, Williams G, van Ofwegen LP (2023) World list of Octocorallia. Helioporidae Moseley, 1876. Accessed through: World Register of Marine Species at: https://www.marinespecies.org/aphia.php?p=taxdetails&id=196193 on 2023–08–07
Mehrotra R, Funesto EG, Arnold S, Pakeenuya S (2017) Toboso biodiversity and ecosystem report - "contrasting areas for priority of protection". Conserv Diver 1–26. https://doi.org/10.13140/RG.2.2.18498.89289
Miyazaki Y, Reimer JD (2015) A new genus and species of octocoral with aragonite calcium-carbonate skeleton (Octocorallia, Helioporacea) from Okinawa, Japan. ZooKeys 511:1–23. https://doi.org/10.3897/zookeys.511.9432
Miyazaki Y, Santos ME, Kunihiro S, Weinstein DK, Reimer JD, Weinstein DK (2016) Rarity of Nanipora kamurai (Anthozoa: Octocorallia: Helioporacea) at its type locality. Marine Biodivers 46(4):917–921. https://doi.org/10.1007/s12526-015-0435-4
Mochizuki A, Hosoda K, Sugiyama M (2015) Distribution and supply mechanisms of high uranium concentration in the rivers of Okinawa Island, Japan. Geocheml J 49:9–14. https://doi.org/10.2343/geochemj.2.0381
Plaza PU, Mehrotra R, Scott CM, Reimer JD (2018) Rare zooxanthellate Nanipora octocoral (Helioporacea) in the Gulf of Thailand. Mar Biodivers 48(4):1961–1967. https://doi.org/10.1007/s12526-017-0705-4
Quattrini AM, Rodríguez E, Faircloth BC, Cowman PF, Brugler MR, Farfan GA, ... McFadden CS (2020) Palaeoclimate ocean conditions shaped the evolution of corals and their skeletons through deep time. Nat Ecol Evol 4(11):1531–1538. doi:https://doi.org/10.1038/s41559-020-01291-1
Ramos AA, Inoue Y, Ohde S (2004) Metal contents in Porites corals: anthropogenic input of river run-off into a coral reef from an urbanized area, Okinawa. Mar Pollut Bull 48:281–294. https://doi.org/10.1016/j.marpolbul.2003.08.003
Reimer JD, Lau YW, Boo WH, Soong K (2018) Living fossil Nanipora (Anthozoa: Octocorallia) as the dominant calcifying benthos in a seagrass meadow in the South China Sea. Matters Select 1–6. https://doi.org/10.19185/matters.201802000001
Reimer JD, Kurihara H, Ravasi T, Ide Y, Izumiyama M, Kayanne H (2021) Unexpected high abundance of aragonite-forming Nanipora (Octocorallia: Helioporacea) at an acidified volcanic reef in southern Japan. Mar Biodivers 51. https://doi.org/10.1007/s12526-021-01165-0
Reimer JD, Fourreau CJ, Yamagiwa H, Poliseno A (2022) First record of Nanipora (Lithotelestidae: Helioporacea: Octocorallia: Anthozoa) from the Yaeyama Islands. Fauna Ryukyuana 63:1–5
Richards ZT, Yasuda N, Kikuchi T, Foster T, Mitsuyuki C, Stat M, Suyama Y, Wilson NG (2018) Integrated evidence reveals a new species in the ancient blue coral genus Heliopora (Octocorallia). Sci Rep 8(15875). https://doi.org/10.1038/s41598-018-32969-z
Schmitt EF, Sluka RD, Sullivan-Sealey KM (2002) Evaluating the use of roving diver and transect surveys to assess the coral reef fish assemblage off southeastern Hispaniola. Coral Reefs 21:216–223. https://doi.org/10.1007/s00338-002-0216-y
Schuhmacher H, Zibrowius H (1985) What is hermatypic? A redefinition of ecological groups in corals and other organisms. Coral Reefs 4:1–9. https://doi.org/10.1007/BF00302198
Wee H, Kobayashi Y, Reimer JD (2021) Effects of temperature, salinity, and depth on Symbiodiniaceae lineages hosted by Palythoa tuberculosa near a river mouth. Mar Ecoly Prog Ser 667:43–60. https://doi.org/10.3354/meps13706
Yang SY, Bourgeois C, Ashworth CD, Reimer JD (2013) Palythoa zoanthid ‘barrens’ in Okinawa: examination of possible environmental causes. Zoological Stud, 52. https://doi.org/10.1186/1810-522X-52-39
Zann L, Bolton L (1985) The distribution, abundance and ecology of the blue coral Heliopora coerulea (Pallas) in the Pacific. Coral Reefs 4:125–134. https://doi.org/10.1007/BF00300871
Acknowledgements
We thank members of the Molecular Invertebrate Systematics and Ecology (MISE) laboratory of the University of the Ryukyus for field work support and discussion. Comments from two anonymous reviewers and the handling editor greatly improved earlier versions of this manuscript.
Funding
GMC was supported by tuition exemptions at the University of the Ryukyus (UR). EAJ and JAAL were supported by Japan Ministry of Education (MEXT) scholarships. Work at Iotorishima was supported by an Okinawa Institute of Science and Technology (OIST) KICKS grant entitled “Japanese volcanic CO2 vents—natural laboratories to study the behaviour and adaptation of marine organisms to acidifying oceans” to JDR and colleagues at UR and OIST. JDR thanks the captain and crew of the Yosemiya III, and cruise members for their support and advice at Iotorishima.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
The authors followed all applicable international, national, and/or institutional guidelines for animal testing, animal care and use of animals.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from Okinawa Prefecture (Permit No. 1504 to JDR).
Data availability
The specimens collected during this study have been deposited in the Fujukan University of the Ryukyus Museum under the corresponding specimen numbers.
Author contribution
GMC and JDR conceived and designed research. GMC, RM, and JDR performed field surveys. GMC, EAJ, and JAAL performed molecular experiments and analyses. GMC wrote the manuscript. All authors edited the manuscript, and all authors read and approved the manuscript.
Additional information
Communicated by B.W. Hoeksema
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Castelló, G.M., Jamodiong, E.A., Lalas, J.A.A. et al. Distribution and molecular phylogeny of the octocoral genus Nanipora (Helioporidae) in the western Pacific. Mar. Biodivers. 53, 73 (2023). https://doi.org/10.1007/s12526-023-01383-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-023-01383-8