The First Records of Pelagic Gastropods Species from the Celebes Sea, North Sulawesi, Indonesia
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Abstract
Despite their weak swimming abilities, which prevent them from swimming against general ocean currents, gastropod larvae can still achieve widespread dispersal. This study aimed to identify pelagic gastropod species, both holoplanktonic and meroplanktonic, and to analyze their distribution in the Celebes Sea. Gastropods were sampled using an Isaacs-Kidd Midwater Trawl (IKMT) during the EWIN 2018 Cruise aboard the R.V. Baruna Jaya VIII LIPI. Species identification relied on morphology and DNA barcoding. Eight holoplanktonic gastropod species were identified: Atlanta inclinata (Atlantidae, Subclass Caenogastropoda), Creseis acicula, Creseis virgula, Boasia chierchiae, Styliola subula (Creseidae), Cavolinia labiata, Telodiacria sp. (Cavoliniidae), and Clio convexa (Cliidae), all belonging to Subclass Heterobranchia. The meroplanktonic species identified, all Caenogastropoda, included Reticutriton pfeifferianus (Cymatiidae), Dulcerana granularis (Bursidae), and Lampasopsis rhodostoma (Bursidae). Most species were found distributed across stations in the eastern and western parts of the Celebes Sea. With the exception of Creseis acicula, Styliola subula, and Reticutriton pfeifferianus, all identified species represent first records for the Celebes Sea. This study marks the first research in the Celebes Sea utilizing morphology and DNA barcoding for identifying pelagic gastropod species, providing a foundational dataset for future investigations.
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References
Amri, K.A., A.A. Atiah, Mutoharoh and D. Ernaningsih. 2015. The Influence of oceanographic parameters on the abundance and distribution of fish larvae in the Celebes Sea. Journal of Indonesian Fisheries Research 21(2): 10–114. (in Indonesian)
Aulina, A., O. Medy, E.Y. Kaligis, N.D.C. Rumampuk, J.R.T.S.L. Rimper and G.S. Gerung. 2023. Gastropods in the tidal of Bulo, Mandolang District, North Sulawesi. Scientific Journal PLATAX 12(1): 177–184. (in Indonesian)
Bandel, K., F. Riedel and H. Tiemann. 1994. A special adaptation to planktonic life in larvae of the Cassoidea (=Tonnoidea) (Gastropoda). Marine Biology 118: 101–108.
Bandel, K., F. Riedel and H. Weikert. 1997. Planktonic gastropods larval, from the Red Sea: a Synopsis. Ophelia 47(3): 151–202.
Barber, P.H., S.R. Palumbi, M.V. Erdmann and M.K. Moosa. 2000. A marine Wallace’s line?” Nature 406: 692–693.
Bednaršek, N., J. Mozˇina, M. Vogt, C. O’Brien and G.A. Tarling. 2012. The global distribution of pteropods and their contribution to carbonate and carbon biomass in the modern ocean. Earth System Science Data 4: 167–186.
Bednaršek, N. and M.D. Ohman. 2015. Changes in pteropod distributions and shell dissolution across a frontal system in the California Current System. Marine Ecology Progress Series 523: 93–103.
Benzie, J.A.H. 1999. Major genetic differences between crown-of-thorns starfish. Biological Bulletin 140: 284–322.
Bucklin, A., K.T.C.A. Peijnenburg, Kosobokova, et al. 2021. Toward a global reference database of CO1 barcodes for marine zooplankton. Marine Biology 168: 78. DOI: 10.1007/s00227-021-03887-y.
Burghardt, L., R. Carvalho, D. Eheberg, G Gerung, F. Kaligis, G. Mamangkey, M. Schrödl, E. Schwabe, V. Vonnemann and H. Wägele. 2006. Molluscan diversity at Bunaken National Park, Sulawesi. Journal of the Zoological Society Wallacea 2: 29–43.
Burridge, A.K., E. Goetze, N. Raes, J. Huisman and K. Peijnenburg. 2015. Global biogeobraphy and evolution of Cuvierina pteropods. BMC Evolutionary Biology 15: 39. DOI: 10.1186/s12862-015-0310-8.
Çağlar, S. and B. Öztürk. 2022. Pelagic gastropods of the Finike Seamounts region, the eastern Mediterranean Sea. Journal Black Sea/Mediterranean Environment 28(2): 204–220.
Castelin, M., J. Lorion, J. Brisset, C. Cruaud, P. Maestrati, J. Utge and S. Samadi. 2012. Speciation patterns in gastropods with long-lived larvae from deep-sea seamounts. Journal Molecular Ecology 21(19): 4828–4853. DOI: 10.1111/j.1365-294X.2012.05743.x.
Collins, R.A. and R.H. Cruickshank. 2013. The seven deadly sins of DNA barcoding. Molecular Ecology Resources 13: 969–975. DOI: 10.1111/1755-0998.12046.
Corse, M.J. Rampal, C. Cuoc, N. Pech, Y. Perez and A. Gilles. 2013. Phylogenetic analysis of Thecosomata blainville, 1824 (Holoplanktonic Opisthobranchia) using morphological and molecular data. PLoS One 8(4): e59439. DOI: 10.1371/journal.pone.0059439.
Dharma, B. 2005. Recent and Fossil Indonesian Shells. Conch Books, Hackenheim, Germany. 424 pp.
Feng, M., N. Zhang, Q. Liu and S. Wijfels. 2018. The Indonesian throughflow, its variability, and centennial change. Geoscience Letters 5: 3. DOI: 10.1186/s40562-018-0102-2.
Folmer, O., M. Black, W. Hoah, R. Lutz and R. Vrijenhoek. 1994. DNA primers for amplication of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Garilli, V., L. Gallettia and D. Parrinello. 2017. Distinct protoconchs recognized in three of the larger Mediterranean Cerithium species (Caenogastropoda: Cerithiidae). Molluscan Research 38: 105–118.
Hall, R., C.A. Motti and F. Kroon. 2017. The Potential Role of the Giant Triton Snail, Charonia tritonis (Gastropoda: Ranellidae) in Mitigating Populations of the Crown-of-Thorns Starfish. Technical Report, Australian Institute of Marine Science, Reef and Rainforest Research Centre Limited, Cairns, Australia. 59 pp.
Hoeksema, B.W. 2007. Delineation of the Indo-Malayan centre of maximum marine biodiversity: the coral triangle. In: Biogeography Time and Place: Distribution, Barriers, and Island (ed. W. Renema), pp. 117–178. Springer, Dordrecht, Netherlands.
Janssen, A.W., L.N. Bush and N. Bednaršek. 2019. The shelled pteropods of the northeast Pacific Ocean (Mollusca: Heterobranchia, Pteropoda). Zoosymposia 13: 305–346.
Jennings, R.M., A. Bucklin, H. Ossenbrügger and R.R. Hopcroft. 2010. Species diversity of planktonic gastropods (Pteropoda and Heteropoda) from six ocean regions based on DNA barcode analysis. Deep Sea Research Part II 57: 2199–2010.
Jitchum, P. and T. Duangdee. 2015. Temporal variation of microzooplankton community in Prasae Estuary, The Gulf of Thailand. Journal of Fisheries and Environment 39: 43–56.
Kaligis, F., J.H. Eisenbart, D. Schillo, et al. 2018. Second survey of heterobranch sea slugs (Mollusca, Gastropoda, Heterobranchia) from Bunaken National Park, North Sulawesi, Indonesia - How much do we know after 12 years?. Marine Biodiversity Records 11: 2. DOI: 10.1186/s41200-018-0136-3.
Kim, M., J.H. Kang and K. Dongsung. 2022. Holoplanktonic and meroplanktonic larvae in the surface waters of the Onnuri Vent Field in the Central Indian Ridge. Journal of Marine Science and Engineering 10(2): 158. DOI: 10.3390/jmse10020158.
Kirkendale, I., G. Hansen, H. Morrison, C. Whisson and N. Wilson. 2019. Molluscs. In: Benthic Habitats and Biodiversity of the Dampier and Montebello Australian Marine Parks (ed. J.K. Keesing), pp. 149–159. Report for the Director of National Parks, CSIRO, Canberra, Australia.
Kochzius, M. and A. Nuryanto. 2008. Strong genetic population structure in the boring giant clam Tridacna crocea across the IndoMalay Archipelago: implications related to evolutionary processes and connectivity. Molecular Ecology 17: 3775–3787.
Lalli, C.M. and R.W. Gilmer. 1989. Pelagic snails. The biology of holoplanktonic Gastropod mollusks. Limnology and Oceanography 34(5): 969–970. DOI: 10.4319/lo.1989.34.5.0969.
Levin, L.A. 2006. Recent progress in understanding larval dispersal: New directions and digressions. Integrative and Comparative Biology 46(3): 282–297. DOI: 10.1093/icb/icj024.
Machida, R.J., Y. Hashiguchi, M. Nishida and S. Nishida. 2009. Zooplankton diversity analysis through single-gene sequencing of a community sample. BMC Genomics 10 (438): 1–7. DOI: 10.1186/1471-2164-10-438.
Marshall, D.J., P.J. Krug, E.K. Kupriyanova, M. Byrne and R.B. Emlet. 2012. The biogeography of marine invertebrate life histories. Annual Reviews of Ecology Evolution and Systematics 43: 97–114.
Morni, M.Z.W., S.A.K.A. Rahi, R. Rumpet, J. Musel and J.R. Hassan. 2017. Checklist of gastropods from the Exclusive Economic Zone (EEZ), Sarawak, Malaysia. Tropical Life Sciences Research 28(1): 117–129.
Ompi, M. 2010. Marine larval invertebrates in ballast waters and marine waters of Bitung Harbor, Lembe Strait of North Sulawesi. Zoo Indonesia 19(1): 37–49. (in Indonesian)
Ompi, M., N. Kawung and C.F.A. Sondak. 2010. An attachment of larval gastropod, Haliotis varia: a laboratorium experiment. Biota 15(3): 407–414. (in Indonesian)
Ompi, M. and I. Svane. 2018. Comparing spawning, larval development, and recruitments of four mussel species (Bivalvia: Mytilidae) from South Australia. AACL Bioflux 11(3): 576–588.
Ompi, M., F. Lumoindong, Y. Tamanampow, N. Undap, A. Papu and H. Wägele. 2019. Monitoring marine Heterobranchia in Lembeh Strait, North Sulawesi (Indonesia), in a changing environment. AACL Bioflux 12(2): 664–677.
Ompi, M., F.B. Boneka, E.Y. Kaligis and S.T. Kaunang. 2023. Settlement of the tropical box mussel, Septifer bilocularis: effects of site, position, and substratum. Aquaculture Research 2023: 4498844. DOI: 10.1155/2023/4498844.
Panchang, R., R. Nigam, F. Riedel, A.W. Janssen and Y.K.U. Hla. 2007. A review of the studies on pteropods from the northern Indian Ocean region with a report on the pteropods of Irrawaddy continental shelf off Myanmar (Burma). Indian Journal of Marine Sciences 36(4): 384–398.
Pappalardo, P., A.G. Collins, K.M.P. Lohan, et al. 2021. The role of taxonomic expertise in interpretation of metabarcoding studies. ICES Journal of Marine Science 78(9): 3397–3410. DOI: 10.1093/icesjms/fsab082.
Puspasari, R., A. Damar, M.M. Kamal and N.N. Wiadyana. 2018. Trophic interaction of fish larvae, phytoplankton, and zooplankton in Pari Island lagoon. IOP Conference Series: Earth and Environmental Science 176: 012020. DOI: 10.1088/1755-1315/176/1/012020.
Rao, N.V.S. and A. Dey. 2000. Catalogue of Marine Molluscs of Andaman and Nicobar Islands. Zoological Survey of India, Kolkata, India. 323 pp.
Rozirwan, Y., H.Y. Sugeha, N. Fitriya, M.R. Firdaus, P. Avianto and I. Iskandar. 2021. Correlation between the phytoplankton distribution with the oceanographic parameters of the deep-sea surface of Sangihe-Talaud, North Sulawesi, Indonesia. IOP Conference Series: Earth and Environmental Science 789: 012007. DOI: 10.1088/1755-1315/789/1/012007.
Sanders, M.T., D. Merle, P. Bouchet, M. Castelin, A. Beu, S. Samadi and N. Puilandre. 2017. One for each ocean: revision of the Bursa granularis (Röding, 1798) species complex (Gastropoda: Tonnoidea: Bursidae). Journal of Molluscan Studies: 83: 384–398.
Sanders, M.T., D. Merle, M. Laurin, C. Bonillo and N. Puillandre. 2021. Raising names from the dead: A time-calibrated phylogeny of frog shells (Bursidae, Tonnoidea, Gastropoda) using Mitogenomic data. Molecular Phylogenetics and Evolution 156: 107040. DOI: 10.1016/j.ympev.2020.107040.
Sani, L.M.I., A. Benyamin, A.K. Husna, D. Arafat, B. Subhan, A. Sunuddin, N. Cakasana, D.F. Lestari and D.F. Madduppa. 2021. A contrasting pattern of reef fish species diversity and diversity and distribution using environmental DNA (eDNA) metabarcoding in longitudinal distance from Jakarta Bay. Journal of Sciences and Tropical Marine Tecnology 13(3): 467–482.
Sawatpeera, S., U.F. Suchart, M. Kruatrachue, Y.P. Chitramvong, P. Sonchaeng, T. Pumthong and J. Nugranad. 2001. Larval development in Haliotis asinina Linnaeus. Journal of Shellfish Research 20(2): 593–601.
Scheltema, R.S. 1971. Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. The Biological Bulletin 140(2): 284–322.
Scheltema, R.S. 1988. Initial evidence for the transport of teleplanic larvae of benthic invertebrates across the East Pacific barrier. Biological Bulletin 174: 145–152.
Simbolon, A.R., M. Ompi, E. Widyastuti and D.A. Wulandari. 2021. DNA Baracoding to Identify Gastropod Larvae (Family Cymatiidae) in the Sangihe-Talaud Islands, North Sulawesi. BAWAL 13(3): 145–155.
Stahlhut, J.K., J. Fernández-Triana, S.J. Adamowicz, M. Buck, H. Goulet, P.D.N. Hebert and M.A. Smith. 2013. DNA barcoding reveals diversity of Hymenoptera and the dominance of parasitoids in a sub-arctic environment. BMC Ecology 13(2): 1–13. DOI: 10.1186/1472-6785-13-2.
Strathmann, R.R. 1993. Hypotheses on the origins of marine larvae. Annual Review of Ecology and Systematics 24: 89–117.
Strathmann, R.R. and D. Grünbaum. 2006. Good eaters, poor swimmers: compromises in larval form. Integrative and Comparative Biology 46(3): 312–322.
Strong, E., N. Puillandre, A.G. Beu, M. Castelin and P. Bouchet. 2019. Frogs and tuns and tritons–A molecular phylogeny and revised family classification of the predatory gastropod superfamily Tonnoidea (Caenogastropoda). Molecular Phylogenetics and Evolution 130: 18–34.
Swearer, S, E, E.A. Treml and J.S. Shima. 2019. A review of biophysical models of marine larval dispersal. Oceanography and Biology: Annual Review 57: 325–356.
Tantanasiriwong, R. 1978. An illustrated checklist of marine shelled gastropods from Phuket Island, adjacent mainland and offshore islands, western peninsular Thailand. Phuket Marine Biological Center Research Bulletin 21: 1–64.
Taufiqurrahman, M., A.J. Wahyudi and Y. Masumoto. 2020. The Indonesian through flow and its impact on geochemistry in the Indonesian seas. ASEAN Journal on Science and Technology for Development 37(1): 29–35.
Tesch, J.J. 1904. The Thecosomata and Gymnosomata of the Siboga-Expedition. Siboga-Expeditie LII. E.J. Brill, Leiden, Nederland. 94 pp.
Tesch, J.J. 1906. Die Heteropoden der Siboga-Expedition. E.J. Brill, Leiden, Netherlands. 112 pp.
Tesch, J.J. 1948. The hecosomatous pteropods. II. The Indo-Pacific. Dana-Report 30: 1–45.
Tucker, A.R. and D.S. Peter. 2000. Compendium of Seashells: A Color Guide to More Than 4,200 of the World’s Marine Shells. El Cason, Calif, Oddysey Publisher, Rolling Hills, USA. 424 pp.
Tunçer, S.N., N. Ogretmen, F. Cakir, A. Oztekin, A. Oral and S.C. Suner. 2021. First record of straight-needle pteropod Creseis acicula Rang, 1828 bloom in the Çanakkale Strait NE Aegean Sea, Turkey. International Journal of Oceanography and Hydrobiology 50(3): 310–324.
Van der Spoel, S. 1973. Clio pyramidata Linnaeus, 1767 forma convexa (Boas, 1886) (Mollusca, Pteropoda). Bulletin Zoologisch Museum 3(3): 15–17.
Wall-Palmer, D., A.K. Burridge, E. Goetze, et al. 2018. Biogeography and genetic diversity of the atlanta heteropods. Progress in Oceanography 160: 1–25.
Wells, F.E., K. Sanpanich, S.K. Tan and T. Duangdee. 2021. The marine and estuarine molluscs of Thailand. Lee Kong Chian Natural History Museum, National University of Singapore. https://lkcnhm.nus.edu.sg/wp-content/uploads/sites/ 10/2021/01/LKCNHM-EBOOK-2021-0001.pdf. Cited 18 Oct 2023.
Wijayanti, L.A.S., N. Fitriya, M.R. Firdaus, T.B. Satriyo, Djumanto, R.Y. Setiawan, N. Nurdin, M. Helmi and M. Zainuddin. 2020. Deep sea phytoplankton community of The Sangihe-Talaud Islands waters. AACL Bioflux 13(5): 3212–3223.
World Register of Marine Species (WoRMS). 2024. World Register of Marine Species. https://www.marinespecies.org/. Cited 18 Oct 2023.
Young, C.M., M.A. Sewel and M.E. Rice. 2002. Atlas of Invertebrate Larvae. AcademicPress: Sandiago, California, USA. 630 pp.
Zhao, B., S. Zhang and P.Y. Qian. 2003. Larval settlement of the silver- or goldlip pearl oyster Pinctada maxima (Jameson) in response to natural biofilms and chemical cues. Aquaculture 220: 883–901.