Integrative taxonomy reveals unanticipated hidden diversity in the monotypic goosefish genus Lophiomus (Teleostei, Lophiidae), with description of three new species and resurrection of Chirolophius laticeps Ogilby, 1910

Keywords: biodiversity, Indo-West Pacific, anglerfish, multigene phylogeny, Tropical Deep-Sea Benthos

Abstract

Thought to be monotypic for decades, the only species in the goosefish genus Lophiomus Gill, Lm. setigerus (Vahl), shows a wide range of morphological variation and is distributed widely in the Indo-West Pacific (IWP). In this study, datasets for two mitochondrial and two nuclear genes sequences obtained from samples of Lophiomus collected in different localities across the IWP were constructed and analyzed to explore the phylogeny and species diversity within the genus. Our integrated approach with multiline evidence unveiled an unanticipated richness of at least six delimited species of Lophiomus. Herein, based on materials already available from museums and new specimens obtained primarily through the Tropical Deep-Sea Benthos program surveying IWP benthic fauna, we formally describe three new species: Lm. immaculioralis sp. nov., Lm. nigriventris sp. nov., and Lm. carusoi sp. nov. Also, we resurrect Lm. laticeps stat. rev. from synonyms of Lm. setigerus. These species can be diagnosed by genetics, body coloration, patterns on the floor of the mouth, peritoneum pigmentation, morphometric measurements, and meristic counts of cranial spines, dorsal-fin spines, and pectoral-fin and pelvic-fin rays from each other and from Lm. setigerus. The species Lm. setigerus, as well as the genus Lophiomus, are re-described accordingly based on the new results. Amended identification keys to the four extant lophiid genera and to species of Lophiomus are also provided.

References

Alcock A.W. 1889. Natural history notes from H.M.’s Indian marine survey steamer ‘Investigator’ no. 12. Descriptions of some new and rare species of fishes from the Bay of Bengal, obtained during the season of 1888–89. Journal of the Asiatic Society of Bengal 3: 296–305.

Bannikov A.F. 2004. The first discovery of an anglerfish (Teleostei, Lophiidae) in the Eocene of the Northern Caucasus. Paleontological Journal 38: 67–72.

Bianchi G. 1985. Field Guide to the Commercial Marine and Brackish-water Species of Tanzania. FAO FAO Species Identification Field Guide for Fishery Purposes, Rome.

Blender Foundation Community. 2018. Blender — A 3D modelling and rendering package. Available from https://www.blender.org [accessed 19 Mar. 2023].

Bloch M.E. & Schneider J.G. 1801. M.E. Blochii, Systema Ichthyologiae Iconibus cx Ilustratum. Sumtibus auctoris impressum et Bibliopolio Sanderiano commissum, Berlin [Berolini]. https://doi.org/10.5962/bhl.title.5750

Borsa P., Hsiao D.-R., Carpenter K.E. & Chen W.-J. 2013a. Cranial morphometrics and mitochondrial DNA sequences distinguish cryptic species of the longface emperor (Lethrinus olivaceus), an emblematic fish of Indo-west pacific coral reefs. Comptes Rendus. Biologies 336 (10): 505–514. https://doi.org/10.1016/j.crvi.2013.09.004

Borsa P., Arlyza I.S., Chen W.-J., Durand J.-D., Meekan M.G. & Shen K.-N. 2013b. Resurrection of New Caledonian maskray Neotrygon trigonoides (Myliobatoidei: Dasyatidae) from synonymy with N. kuhlii, based on cytochrome-oxidase I gene sequences and spotting patterns. Comptes Rendus. Biologies 336 (4): 221–232. https://doi.org/10.1016/j.crvi.2013.05.005

Borsa P., Sembiring A., Fauvelot C. & Chen W.-J. 2014. Resurrection of Indian Ocean humbug damselfish, Dascyllus abudafur (Forsskål) from synonymy with its Pacific Ocean sibling, Dascyllus aruanus (L.). Comptes Rendus. Biologies 337 (12): 709–716. https://doi.org/10.1016/j.crvi.2014.09.001

Bouchet P., Héros V., Lozouet P. & Maestrati P. 2008. A quarter-century of deep-sea malacological exploration in the south and West Pacific: where do we stand? How far to go. In: Héros V., Cowie R.H. & Bouchet P. (eds) Tropical Deep-sea Benthos 25: 9–40. Muséum national d’Histoire naturelle, Paris.

Carnevale G. & Pietsch T.W. 2012. †Caruso, a new genus of anglerfishes from the Eocene of Monte Bolca, Italy, with a comparative osteology and phylogeny of the teleost family lophiidae. Journal of Systematic Palaeontology 10 (1): 47–72. https://doi.org/10.1080/14772019.2011.565083

Caruso J.H. 1981. The systematics and distribution of the lophiid anglerfishes: I. A revision of the genus Lophiodes with the description of two new species. Copeia 1981 (3): 522–549. https://doi.org/10.2307/1444556

Caruso J.H. 1983. The systematics and distribution of the lophiid anglerfishes: II. Revisions of the genera Lophiomus and Lophius. Copeia 1983 (1): 11–30. https://doi.org/10.2307/1444694

Caruso J.H. 1985. The systematics and distribution of the lophiid anglerfishes: III. Intergeneric relationships. Copeia 1985 (4): 870–875. https://doi.org/10.2307/1445235

Caruso J.H. 1986. Lophiidae. In: Smith M.M. & Heemstra P.C. (eds) Smiths’ Sea Fishes: 363–366. Springer-Verlag, Berlin.

Chen W.-J. & Borsa P. 2020. Diversity, phylogeny, and historical biogeography of large-eye seabreams (Teleostei: Lethrinidae). Molecular Phylogenetics and Evolution 151: e106902. https://doi.org/10.1016/j.ympev.2020.106902

Dayrat B. 2005. Towards integrative taxonomy. Biological Journal of the Linnean society 85 (3): 407–417. https://doi.org/10.1111/j.1095-8312.2005.00503.x

De la Cruz-Agüero J., Galván-Magaña F., Abitia-Cárdenas L.A., Rodríguez-Romero J. & Gutiérrez-Sánchez F.J. 1994. Systematic list of marine fishes from Bahia Magdalena, Baja California Sur (Mexico). Ciencias Marinas 20: 17–31. https://doi.org/10.7773/cm.v20i1.956

Fischer W., Sousa I., Silva C., de Freitas A., Poutiers J.M., Schneider W., Borges T.C., Feral J.P. & Massinga A. 1990. Guia de Campo das Espécies comerciais marinhas e de Águas salobras de Moçambique. Fichas FAO de Identificaçao de Espécies para Actividades de Pesca, Rome.

Fricke R., Eschmeyer W.N. & van der Laan R. 2022. Eschmeyer’s Catalog of Fishes: Genera, Species, References. Available from https://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp [accessed 23 Apr. 2023].

Gill T.N. 1883. Supplementary note on the Pediculati. Proceedings of the United States National Museum 5: 551–556. Available from https://www.biodiversitylibrary.org/page/7321063 [accessed 23 Apr. 2023].

Golani D. & Bogorodsky S.V. 2010. The fishes of the Red Sea — Reappraisal and updated checklist. Zootaxa 2463: 1–135. https://doi.org/10.11646/zootaxa.2463.1.1

Guindon S., Dufayard J.-F., Lefort V., Anisimova M., Hordijk W. & Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 Systematic Biology 59 (3): 307–321. https://doi.org/10.1093/sysbio/syq010

Haring P. & Maguire J. 2008. The monkfish fishery and its management in the northeastern USA. ICES Journal of Marine Science 65 (7): 1370–1379. https://doi.org/10.1093/icesjms/fsn131

Ho H.-C. & Chen W.-J. 2013. DNA sequences and morphological variation in Lophiodes iwamotoi Ho, Serét & Shao, 2011 based on new material from New Caledonia. Zootaxa 3682: 594–598. https://doi.org/10.11646/zootaxa.3682.4.12

Ho H.-C., Séret B. & Shao K.-T. 2011. Records of anglerfishes (Lophiiformes: Lophiidae) from the western South Pacific Ocean, with descriptions of two new species. Journal of Fish Biology 79: 1722–1745. https://doi.org/10.1111/j.1095-8649.2011.03106.x

Ho H.-C., Bineesh K.K. & Akhilesh K.V. 2014. Rediscovery of Lophiodes triradiatus (Lloyd, 1909), a senior synonym of L. infrabrunneus Smith and Radcliffe (Lophiiformes: Lophiidae). Zootaxa 3786: 587–592. https://doi.org/10.11646/zootaxa.3786.5.6

Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q. & Vinh L.S. 2017. UFboot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution 35 (2): 518–522. https://doi.org/10.1093/molbev/msx281

Huang C.-S. 2015. Molecular Systematics of the Lophiidae, Ogcocephalidae, and Chaunacidae (Lophiiformes) occurring in Western Pacific Ocean. Master thesis, National Taiwan University.

Hung K.-W., Russell B.C. & Chen W.-J. 2017. Molecular systematics of threadfin breams and relatives (Teleostei, Nemipteridae). Zoologica Scripta 46 (5): 536–551. https://doi.org/10.1111/zsc.12237

Ivanova N., Zemlak T., Hanner R. & Hebert P. 2007. Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes 7 (4): 544–548. https://doi.org/10.1111/j.1471-8286.2007.01748.x

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A. & Jermiin L.S. 2017. Modelfinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285

Katoh K., Rozewicki J. & Yamada K.D. 2019. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20 (4): 1160–1166. https://doi.org/10.1093/bib/bbx108

Kekkonen M. & Hebert P.D. 2014. DNA barcode-based delineation of putative species: efficient start for taxonomic workflows. Molecular Ecology Resources 14 (4): 706–715. https://doi.org/10.1111/1755-0998.12233

Khalaf M.A. 2004. Fish fauna of the Jordanian Coast, Gulf of Aqaba, Red Sea. Journal of King Abdulaziz University: Marine Sciences 15 (1): 23–50.

Kikinis R., Pieper S.D. & Vosburgh K.G. 2014. 3D Slicer: A platform for subject-specific image analysis, visualization, and clinical support. In: Jolesz F. (ed.) Intraoperative Imaging and Image-Guided Therapy: 277–289. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7657-3_19

Kulbicki M., Randall J.E. & Rivaton J. 1994. Checklist of the fishes of the Chesterfield islands (Coral Sea). Micronesica 27: 1–43.

Lee S.-H., Lee M.-Y., Matsunuma M. & Chen W.-J. 2019. Exploring the phylogeny and species diversity of Chelidoperca (Teleostei: Serranidae) from the western Pacific Ocean by an integrated approach in systematics, with descriptions of three new species and a redescription of C. lecromi Fourmanoir, 1982. Frontiers in Marine Science 6: 1–26. https://doi.org/10.3389/fmars.2019.00465

Leslie R.W. & Grant W.S. 1991. Redescription of the Southern African Anglerfish Lophius vomerinus Valenciennes, 1837 (Lophiiformes: Lophiidae). Copeia 1991 (3): 787–800. https://doi.org/10.2307/1446406

Lo P.C., Liu S.H., Nor S.A.M. & Chen W.-J. 2017. Molecular exploration of hidden diversity in the Indo-West Pacific sciaenid clade. PLoS ONE 12 (7): e0176623. https://doi.org/10.1371/journal.pone.0176623

Love M.S., Bizzarro J.J., Cornthwaite A.M., Frable B.W. & Maslenikov K.P. 2021. Checklist of marine and estuarine fishes from the Alaska–Yukon Border, Beaufort Sea, to Cabo San Lucas, Mexico. Zootaxa 5053 (1): 1–285. https://doi.org/10.11646/zootaxa.5053.1.1

Minh B.Q., Nguyen M.A.T. & von Haeseler A. 2013. Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30 (5): 1188–1195. https://doi.org/10.1093/molbev/mst024

Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., von Haeseler A. & Lanfear R. 2020. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37 (5): 1530–1534. https://doi.org/10.1093/molbev/msaa015

Miya M., Pietsch T.W., Orr J.W., Arnold R.J., Satoh T.P., Shedlock A.M. Ho H.-C., Shimazaki M., Yabe M. & Nishida M. 2010. Evolutionary history of anglerfishes (Teleostei: Lophiiformes): a mitogenomic perspective. BMC Evolutionary Biology 10: 1–27. https://doi.org/10.1186/1471-2148-10-58

Ni Y., Wu H.-L. & Li S. 2012. A new species of the genus Sladenia (Pisces, Lophiidae) from the East China Sea and South China Sea. Acta Zootaxonomica Sinica 37 (1): 211–216.

Ogilby J.D. 1910. On some new fishes from the Queensland coast. Endeavour Series, No. 1. The Proceedings of the Royal Society of Queensland 23: 85–139. https://doi.org/10.5962/p.351378

Pietsch T. 1984. Lophiiformes: Development and relationships. In: Moser H. et al. (eds) Ontogeny and Systematics of Fishes. Special Publication 1: 320–325. American Society of Ichthyologists and Herpetologists, Lawrence, KS.

Pietsch T. 2009. Oceanic Anglerfishes. Extraordinary Diversity in the Deep Sea. University of California Press, Berkeley, CA. https://doi.org/10.1525/9780520942554

Pietsch T. & Carnevale G. 2011. A new genus and species of lophiid anglerfish (Teleostei: Lophiiformes) from the Eocene of Monte Bolca, Italy. Copeia 2011: 64–71. https://doi.org/10.1643/CI-10-080

Puillandre N., Brouillet S. & Achaz G. 2020. ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21 (2): 609–620. https://doi.org/10.1111/1755-0998.13281

Ratnasingham S. & Hebert P.D.N. 2007. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7: 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x

R Core Team. 2022. R: A language and environment for statistical computing. Ver. 4.2.1 Available from https://www.r-project.org/ [accessed 19 Mar. 2022].

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029

Samuel C.T. 1963. Bottom fishes collected by R.V. Conch off the Kerala coast. Bulletin of the Department of Marine Biology Oceanogrphy, University of Kerala 1: 97–121.

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Prebisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.-Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P. & Cardona A. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9: 676–682. https://doi.org/10.1038/nmeth.2019

Sommer C., Schneider W. & Poutiers J.-M. 1996. The Living Marine Resources of Somalia. FAO Species Identification Field Guide for Fishery Purposes, Rome.

Tamura K., Stecher G. & Kumar S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38 (7): 3022–3027. https://doi.org/10.1093/molbev/msab120

Tanaka S. 1918. Twelve new species of Japanese fishes. Dobutsugaku Zasshi 30: 223–227.

Vahl M. 1797. Beskrivelse tvende nye arter af bredflab-slaegten Lophius. Skrivter af Naturhistorie-Selskabet Kiøbenhavn 4: 212–216. Available from https://www.biodiversitylibrary.org/page/58273971 [accessed 19 Mar. 2023].

Ward R.D. 2009. DNA barcode divergence among species and genera of birds and fishes. Molecular Ecology Resources 9: 1077–1085. https://doi.org/10.1111/j.1755-0998.2009.02541.x

Ward R.D., Zemlak T.S., Innes B.H., Last P.R. & Hebert P.D. 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society B: Biological Sciences 360 (1462): 1847–1857. https://doi.org/10.1098/rstb.2005.1716

Zemlak T.S., Ward R.D., Connell A.D., Holmes B.H. & Hebert P.D.N. 2009. DNA barcoding reveals overlooked marine fishes. Molecular Ecology Resources 9: 237–242. https://doi.org/10.1111/j.1755-0998.2009.02649.x

Zhang J., Kapli P., Pavlidis P. & Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29 (22): 2869–2876. https://doi.org/10.1093/bioinformatics/btt499

Published
2024-07-15
How to Cite
Chen, H.-P., Lee, M.-Y., & Chen, W.-J. (2024). Integrative taxonomy reveals unanticipated hidden diversity in the monotypic goosefish genus Lophiomus (Teleostei, Lophiidae), with description of three new species and resurrection of Chirolophius laticeps Ogilby, 1910 . European Journal of Taxonomy, 943(1), 239–287. https://doi.org/10.5852/ejt.2024.943.2599
Section
Research article