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A new lacustrine ricefish from central Sulawesi, with a redescription of Oryzias marmoratus (Teleostei: Adrianichthyidae)

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Abstract

Oryzias loxolepis, new species, is described from Lake Towuti in the Malili Lake system, central Sulawesi, Indonesia. Historically this new species has been confused with Oryzias marmoratus (Aurich 1935), which we redescribe. While both species share dark brown blotches on a grayish-brown trunk, O. loxolepis differs from O. marmoratus in having 11 abdominal vertebrae, 12 or 13 transverse scales, a shorter caudal peduncle, terminal mouth, reduced nuchal concavity, slanted trunk scales, and a rounded male dorsal fin. Oryzias loxolepis can be also distinguished from Oryzias profundicola Kottelat 1990, another sympatric congener in Lake Towuti, in having a longer snout in both sexes, in males in having a larger head and eyes, and a black margined dorsal fin, and in females in having a shallower body depth at the anal- and dorsal-fin origins. A phylogenetic analysis based on genome-wide single nucleotide variants reveals O. loxolepis to be a sister taxon to O. profundicola rather than O. marmoratus. The identities of specimens historically referred to “O. marmoratus” in previous genetic studies are re-evaluated.

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References

  • Ahmad W (1978) Geology along the Matano fault zone, East Sulawesi, Indonesia. In: Wiryosujono S, Sudrajat A (eds) Proceedings: Regional Conference on the Geology and Mineral Resources of South East Asia, Jakarta, Indonesia, 4–7 August 1975. Indonesian Association of Geologists, Jakarta, pp 143–150

  • Ansai S, Mochida K, Fujimoto S, Mokodongan DF, Sumarto BKA, Masengi KWA, Hadiaty RK, Nagano AJ, Toyoda A, Naruse K, Yamahira K, Kitano J (2021) Genome editing reveals fitness effects of a gene for sexual dichromatism in Sulawesian fishes. Nat Commun 12:1350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aurich H (1935) Mitteilung der Wallacea-Expedition Woltereck. Mitteilung XIII. Fische I. Zool Anz 112:97–107

    Google Scholar 

  • Aurich H (1938) Mitteilung XXVIII der Wallacea-Expedition Woltereck. Die Gobiiden (Ordnung: Gobioidea). Int Rev Gesamten Hydrobiol Hydrogr 38:125–183

    Article  Google Scholar 

  • Bleeker P (1854) Ichthyologische waarnemingen, gedaan op verschillende reizen in de residentie Banten. Nat Tijdschr Ned Ind 7:309–326

    Google Scholar 

  • Boulenger G (1897) An account of the freshwater fishes collected in Celebes by Drs P. and F. Sarasin. Proc Zool Soc London 1897:426–429, pl 28

  • Brembach M (1982) Drei neue Dermogenys-Arten aus Sulawesi: D. montanus, D. vogti, D. megarrhamphus. Die Aquarien- und Terrarienzeitschrift 5(2):51–55

  • Brooks JL (1950) Speciation in ancient lakes. Q Rev Biol 25:131–176

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890

    Article  PubMed  PubMed Central  Google Scholar 

  • Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, Whitwham A, Keane T, McCarthy SA, Davies RM, Li H (2021) Twelve years of SAMtools and BCFtools. GigaScience 10:giab008

  • Gani A, Suhendra N, Herder F, Schwarzer J, Möhring J, Montenegro J, Herjayanto M, Mokodongan DF (2022) A new endemic species of pelvic-brooding ricefish (Beloniformes: Adrianichthyidae: Oryzias) from Lake Kalimpa’a, Sulawesi, Indonesia. Bonn Zool Bull 71:77–85

    Google Scholar 

  • Hall R (2011) Australia-SE Asia collision: plate tectonics and crustal flow. In: Hall R, Cottam MA, Wilson MEJ (eds) The Southeast Asian Gateway: history and tectonics of Australia-Asia collision. The Geological Society of London, London, pp 75–109

    Google Scholar 

  • Hall R (2012) Sundaland and Wallacea: geology, plate tectonics and palaeogeography. In: Gower DJ, Johnson KG, Richardson JE, Rosen BR, Rüber L, Williams S (eds) Biotic evolution and environmental change in Southeast Asia. Cambridge University Press, Cambridge, pp 32–78

    Chapter  Google Scholar 

  • Herder F, Chapuis S (2010) Oryzias hadiatyae, a new species of ricefish (Atherinomorpha: Beloniformes: Adrianichthyidae) endemic to Lake Masapi, Central Sulawesi, Indonesia. Raffles Bull Zool 58:269–280

    Google Scholar 

  • Herder F, Hadiaty RK, Nolte AW (2012) Pelvic-fin brooding in a new species of riverine ricefish (Atherinomorpha: Beloniformes: Adrianichthyidae) from Tana Toraja, Central Sulawesi, Indonesia. Raffles Bull Zool 60:467–476

    Google Scholar 

  • Herder F, Schwarzer J, Pfaender J, Hadiaty RK, Schliewen UK (2006) Preliminary checklist of sailfin silversides (Teleostei: Telmatherinidae) in the Malili Lakes of Sulawesi (Indonesia), with a synopsis of systematics and threats. Verhandl Gesell Ichthyol 5:139–163

    Google Scholar 

  • Herre AWCT, Ablan GL (1934) Aplocheilus luzonensis, a new Philippine cyprinodont. Philipp J Sci 54: 275–277

    Google Scholar 

  • Herzeel C, Costanza P, Decap D, Fostier J, Wuyts R, Verachtert W (2021) Multithreaded variant calling in elPrep 5. PLoS ONE 16:e0244471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilgers L, Hartmann S, Pfaender J, Lentge-Maaß N, Marwoto RM, von Rintelen T, Hofreiter M (2022) Evolutionary divergence and radula diversification in two ecomorphs from an adaptive radiation of freshwater snails. Genes 13:1029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoese DF, Hadiaty RK, Herder F (2015) Review of the dwarf Glossogobius lacking head pores from the Malili Lakes, Sulawesi, with a discussion of the definition of the genus. Raffles Bull Zool 63:14–26

    Google Scholar 

  • Ishikawa Y (1994) Innervation of lateral line system in the medaka, Oryzias latipes. Fish Biol J Medaka 6:17–24

    Google Scholar 

  • Kakioka R, Sutra N, Kobayashi H, Ansai S, Masengi KWA, Nagano AJ, Okuda N, Tanaka R, Sato M, Yamahira K (2021) Resource partitioning is not coupled with assortative mating in sympatrically divergent ricefish in a Wallacean ancient lake. J Evol Biol 34:1133–1143

    Article  CAS  PubMed  Google Scholar 

  • Klotz W, von Rintelen T, Wowor D, Lukhaup C, von Rintelen K (2021) Lake Poso's shrimp fauna revisited: the description of five new species of the genus Caridina (Crustacea, Decapoda, Atyidae) more than doubles the number of endemic lacustrine species. ZooKeys 1009:81–122

    Article  PubMed  PubMed Central  Google Scholar 

  • Kottelat M (1990a) Synopsis of the endangered Buntingi (Osteichthyes: Adrianichthyidae and Oryziidae) of Lake Poso, Central Sulawesi, Indonesia, with a new reproductive guild and descriptions of three new species. Ichthyol Explor Freshw 1:49–67

  • Kottelat M (1990b) The ricefishes (Oryziidae) of the Malili Lakes, Sulawesi, Indonesia, with description of a new species. Ichthyol Explor Freshw 1:151–166

  • Kottelat M (1990c) Sailfin silversides (Pisces: Telmatherinidae) of Lakes Towuti, Mahalona and Wawontoa (Sulawesi, Indonesia) with descriptions of two new genera and two new species. Ichthyol Explor Freshw 1:227–246

  • Kottelat M (2013) The fishes of the inland waters of Southeast Asia: a catalogue and core bibliography of the fishes known to occur in freshwaters, mangroves and estuaries. Raffles Bull Zool (Suppl) 27:1–663

    Google Scholar 

  • Kottelat M, Whitten T, Kartikasari SN, Wirjoatmodjo S (1993) Freshwater fishes of Western Indonesia and Sulawesi. Periplus Editions, Hong Kong

    Google Scholar 

  • Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larson H (2001) A revision of the gobiid fish genus Mugilogobius (Teleostei: Gobioidei), and its systematic placement. Rec West Aust Mus Suppl 62:1–233

    Article  Google Scholar 

  • Larson HK, Geiger MF, Hadiaty RK, Herder F (2014) Mugilogobius hitam, a new species of freshwater goby (Teleostei: Gobioidei: Gobiidae) from Lake Towuti, central Sulawesi, Indonesia. Raffles Bull Zool 62:718–725

    Google Scholar 

  • Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997v2 [q-bio.GN]

  • Magtoon W (2010) Oryzias songkhramensis, a new species of ricefish (Beloniformes: Adrianichthyidae) from northeast Thailand and central Laos. Trop Nat Hist 10:107–129

    Google Scholar 

  • Mandagi IF, Mokodongan DF, Tanaka R, Yamahira K (2018) A new riverine ricefish of the genus Oryzias (Beloniformes, Adrianichthyidae) from Malili, Central Sulawesi, Indonesia. Copeia 2018:297–304

    Article  Google Scholar 

  • Mandagi IF, Kakioka R, Montenegro J, Kobayashi H, Masengi KWA, Inomata N, Nagano AJ, Toyoda A, Ansai S, Matsunami M, Kimura R, Kitano J, Kusumi J, Yamahira K (2021) Species divergence and repeated ancient hybridization in a Sulawesian lake system. J Evol Biol 34:1767–1780

    Article  CAS  PubMed  Google Scholar 

  • Mokodongan DF, Yamahira K (2015) Origin and intra-island diversification of Sulawesi endemic Adrianichthyidae. Mol Phylogenet Evol 93:150–160

    Article  PubMed  Google Scholar 

  • Mokodongan DF, Tanaka R, Yamahira K (2014) A new ricefish of the genus Oryzias (Beloniformes, Adrianichthyidae) from Lake Tiu, Central Sulawesi, Indonesia. Copeia 2014:561–567

    Article  Google Scholar 

  • Nakae M, Asaoka R, Wada H, Sasaki K (2012) Fluorescent dye staining of neuromasts in live fishes: an aid to systematic studies. Ichthyol Res 59:286–290

    Article  Google Scholar 

  • Ortiz EM (2019) vcf2phylip v2.0: convert a VCF matrix into several matrix formats for phylogenetic analysis. Zenodo. https://doi.org/10.5281/zenodo.2540861

  • Parenti LR (2008) A phylogenetic analysis and taxonomic revision of ricefishes, Oryzias and relatives (Beloniformes, Adrianichthyidae). Zool J Linn Soc 154:494–610

    Article  Google Scholar 

  • Parenti LR, Hadiaty RK (2010) A new remarkably colorful, small ricefish of the genus Oryzias (Beloniformes, Adrianichthydae) from Sulawesi, Indonesia. Copeia 2010:268–273

    Article  Google Scholar 

  • Parenti LR, Soeroto B (2004) Adrianichthys roseni and Oryzias nebulosus, two new ricefishes (Atherinomorpha: Beloniformes: Adrianichthyidae) from Lake Poso, Sulawesi, Indonesia. Ichthyol Res 51:10–19

    Article  Google Scholar 

  • Parenti LR, Hadiaty RK, Lumbantobing D, Herder F (2013) Two new ricefishes of the genus Oryzias (Atherinomorpha: Beloniformes: Adrianichthyidae) augment the endemic freshwater fish fauna of southeastern Sulawesi, Indonesia. Copeia 2013:403–414

    Article  Google Scholar 

  • Pfaender J, Hadiaty RK, Schliewen UK, Herder F (2016) Rugged adaptive landscapes shape a complex, sympatric radiation. Proc R Soc B Biol Sci 283:2015–2342

    Google Scholar 

  • Poettinger T, Schubart CD (2014) Molecular diversity of freshwater crabs from Sulawesi and the sequential colonization of ancient lakes. Hydrobiologia 739:73–84

    Article  CAS  Google Scholar 

  • Popta CML (1905) Haplochilus sarasinorum, n. sp. Notes Leyden Mus 25:239–247

    Google Scholar 

  • Roberts TR, Chakraborty P, Yardi K, Mukherjee P (2021) Oryzias andrewi, new species of slender ricefish from Bengal, India, related to the highly specialized western indian coastal Horaichthys setnai Kulkarini 1940 (Cyprinodontiformes, Adrianichthyidae). Aqua, Int J Ichthyol 27:21–35

    Google Scholar 

  • Russell JM, Vogelb H, Bijaksanac S, Mellesd M, Deinoe A, Hafidzc A, Haffnerf D, Hasbergd AKM, Morlockb M, von Rinteleng T, Shepparda R, Stelbrinkh B, Stevensoni J (2020) The late quaternary tectonic, biogeochemical, and environmental evolution of ferruginous Lake Towuti, Indonesia. Paleogeogr Paleoclimatol Paleoecol 556:109905

    Article  Google Scholar 

  • Sabaj MH (2022) Codes for Natural History Collections in Ichthyology and Herpetology (online supplement). Version 9.0 (14 February 2022). American Society of Ichthyologists and Herpetologists, Washington, D.C. https://asih.org/standard-symbolic-codes. Accessed 16 December 2022

  • Seleit A, Ansai S, Yamahira K, Masengi KWA, Naruse K, Centanin L (2021) Diversity of lateral line patterns and neuromast numbers in the genus Oryzias. J Exp Biol 224:jeb242490

  • Sumarto BKA, Kobayashi H, Kakioka R, Tanaka R, Maeda K, Tran HD, Koizumi N, Morioka S, Bounsong V, Watanabe K, Musikasinthorn P, Tun S, Yun LKC, Anoop VK, Raghavan R, Masengi KWA, Fujimoto S, Yamahira K (2020) Latitudinal variation in sexual dimorphism in a freshwater fish group. Biol J Linn Soc 131:898–908

    Article  Google Scholar 

  • Takehana Y, Naruse K, Sakaizumi M (2005) Molecular phylogeny of the medaka fishes genus Oryzias (Beloniformes: Adrianichthyidae) based on nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol 36:417–428

    Article  CAS  PubMed  Google Scholar 

  • Utama IV, Mandagi IF, Lawelle SA, Masengi KWA, Watanabe K, Sawada N, Nagano AJ, Kusumi J, Yamahira K (2022) Deeply divergent freshwater fish species within a single river system in central Sulawesi. Mol Phylogenet Evol 173:107519

    Article  PubMed  Google Scholar 

  • van der Auwera GA, O'Connor BD (2020) Genomics in the Cloud: using Docker, GATK, and WDL in Terra (1st Edition). O'Reilly Media, California

  • von Rintelen T, von Rintelen K, Glaubrecht M, Schubart CD, Herder F (2012) Aquatic biodiversity hotspots in Wallacea: the species flocks in the ancient lakes of Sulawesi, Indonesia. In: Gower D, Johnson K, Richardson J, Rosen B, Rüber L, Williams S (eds) Biotic evolution and environmental change in Southeast Asia. Cambridge Univ Press, Cambridge, pp 290–315

    Chapter  Google Scholar 

  • Wallace AR (1876) The geographical distribution of animals. Harper & Brothers, New York

    Google Scholar 

  • Wasiljew BD, Pfaender J, Wipfler B, Gabelaia M, Utama IV, Wantania LL, Herder F (2021) Sexual dimorphism in an adaptive radiation: does intersexual niche differentiation result in ecological character displacement? Ecol Evol 11:14615–14629

    Article  PubMed  PubMed Central  Google Scholar 

  • Weber M (1894) Die Süsswasser-Fische des Indischen Archipels, nebst Bemerkungen über den Ursprung der Fauna von Celebes. Zool Ergebn Reise Niederl Ost-Indien 3:405–476, pls 17–22

  • Weber M, de Beaufort LF (1922) The fishes of the Indo-Australian Archipelago vol. 4. Heteromi, Solenichthyes, Synentognathi, Percesoces, Labyrinthici, Microcyprini. E. J. Brill, Leiden

  • Whitten AJ, Mustafa M, Henderson GS (2002) The ecology of Sulawesi. Periplus, Singapore

  • Yamahira K, Ansai S, Kakioka R, Yaguchi H, Kon T, Montenegro J, Kobayashi H, Fujimoto S, Kimura R, Takehana Y, Setiamarga DHE, Takami Y, Tanaka R, Maeda K, Tran HD, Koizumi N, Morioka S, Bounsong V, Watanabe K, Musikasinthorn P, Tun S, Yun LKC, Masengi KWA, Anoop VK, Raghavan R, Kitano J (2021) Mesozoic origin and ‘out-of-India’ radiation of ricefishes (Adrianichthyidae). Biol Lett 17:20210212

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamahira K, Mokodongan DF, Konishi M, Mandagi IF, Masengi KWA, Lawelle SA, Kusumi J, Inomata N (2023) Discovery of a genetically distinct lineage in medaka species within Lake Towuti in central Sulawesi. Ichthyol Res 70:185–189

    Article  Google Scholar 

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Acknowledgments

We thank I.F. Mandagi (Sam Ratulangi Univ.), B. Soeroto (Sam Ratulangi Univ.), S.A. Lawelle (Halu Oleo Univ.), K. Mochida (Nagasaki Inst. Appl. Sci.), J. Montenegro (JAMSTEC), R. Kakioka (Univ. Ryukyus), S. Ansai (Tohoku Univ.), and local villagers in Timampu (Bapak-Ryan and his families) for assistance with our field collections; H.H. Tan (ZRC) for providing radiographs; H.H. Tan and M. Kottelat (ZRC) for providing valuable comments for our manuscript; R. Kakioka for help and valuable comments for our phylogenomic analysis; Y. Takehana (Nagahama Inst. Bio.) for providing mitochondrial sequences; N. Hashimoto (freelance photographer) and K. Mochida for providing live photographs; M. Sato (NSMT) providing equipments for fluorescent staining of neuromasts; H.H. Tan, K.P. Lim, and P.K.L. Ng (ZRC), T. Naruse (Univ. Ryukyus), I.V. Utama (Univ. Ryukyus, MZB), R.K. Hadiaty (MZB), E. Dondorp (Naturalis), J. McLane (BMNH), K. Maeda (Okinawa Inst. Sci. Technol.), H. Senou (KPM), M. Nakae, H. Hata, and G. Shinohara (NSMT) for access to museum collections; T. von Rintelen (ZMB) for providing the original map. We also thank S. O’Shea (Edanz Co. Ltd.) for editing a draft of this manuscript. We are grateful the Ministry of Research, Technology, and Higher Education, Republic of Indonesia (RISTEKDIKTI) and the Faculty of Fisheries and Marine Science, Sam Ratulangi University, for the permit to conduct research in Sulawesi (research permit numbers 107/SIP/FRP/E5/Dit.KI/IV/2018). All experiments were approved by the Animal Care Committee of the University of the Ryukyus (201899). This study was supported by JSPS KAKENHI to HK (19J22686) and KY (17H01675 and 21H04782).

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Authors and Affiliations

  1. Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, 903-0213, Japan

    Hirozumi Kobayashi, Mizuki Horoiwa & Kazunori Yamahira

  2. Museum Zoologicum Bogoriense, Research Center for Biology, National Research and Innovation Agency, Cibinong, 16911, Indonesia

    Daniel F. Mokodongan

  3. Research Laboratory Center, Faculty of Medicine, University of the Ryukyus, Okinawa, 903-0213, Japan

    Shingo Fujimoto

  4. World’s Medaka Aquarium, Nagoya Higashiyama Zoological Park, Nagoya, 464-0804, Japan

    Rieko Tanaka

  5. Faculty of Fisheries and Marine Science, Sam Ratulangi University, Manado, 95115, Indonesia

    Kawilarang W. A. Masengi

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  1. Hirozumi Kobayashi
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  3. Mizuki Horoiwa
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  4. Shingo Fujimoto
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Correspondence to Hirozumi Kobayashi or Kazunori Yamahira.

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Kobayashi, H., Mokodongan, D.F., Horoiwa, M. et al. A new lacustrine ricefish from central Sulawesi, with a redescription of Oryzias marmoratus (Teleostei: Adrianichthyidae). Ichthyol Res 70, 490–514 (2023). https://doi.org/10.1007/s10228-023-00908-2

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