Skip to main content
SpringerLink
Log in

Identification of five species of Dendrodoris (Mollusca: Nudibranchia) from Japan, using DNA barcode and larval characters

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

Species of the genus Dendrodoris are defined as “radula-less” dorids (Nudibranchia: Doridina: Porostomata: Dendrodorididae). These sea slugs are colorful nudibranchs distributed across the world’s oceans. Because of color variations and anatomical similarities, species discrimination has been disputed in several Dendrodoris species. We determined the partial mitochondrial COI gene sequences and 18S rRNA gene sequences of five Dendrodoris species (D. arborescens, D. denisoni, D. guttata, D. nigra, and D. rubra) and Doriopsilla miniata in Japan to clarify the species identity of each dendrodorid species. We examined a total of 50 specimens from the intertidal zone at 10 sites in four regions along the Pacific coast of Japan. Partial COI gene sequences significantly differed among the six species. Although six partial 18S rRNA gene sequences were obtained for the six species, sequences differed little among species and did not clarify details of the Dendrodoris phylogeny. We also described the morphological features of veliger larvae of three Dendrodoris species. (D. arborescens, D. guttata, and D. rubra) The veligers of D. arborescens had a brown-pigmented, cup-shaped shell, and its foot was not retracted into the shell. In contrast, the veligers of D. guttata and D. rubra had a transparent, coiled shell with an operculum. Mean shell lengths of D. arborescens, D. rubra, and D. guttata were 171.5 ± 8.0, 172.8 ± 4.9, and 222.3 ± 15.2 μm, respectively. The present molecular analysis and larval characteristics indicated that each of the six species is a distinct species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Apte D, Bhave V, Parasharya D (2010) An annotated and illustrated checklist of the opisthobranch fauna of gulf of Kutch, Gujarat, India with 21 new records for Gujarat and 13 new records for India: Part 1. J Bomb Nat Hist Soc 107:14–23

    Google Scholar 

  • Baba K (1949) Opisthobranchia of Sagami Bay: collected by His majesty the emperor of Japan. Iwanami Shoten, Tokyo

    Google Scholar 

  • Barash A, Danin Z (1986) Further additions to the knowledge of Indo-Pacific molluscs in the Mediterranean Sea. Spixiana 9:117–141

    Google Scholar 

  • Behrens DW, Valdés A (2004) A new species of Dendrodoris (Mollusca: Nudibranchia: Dendrodorididae) from the Pacific Coast of North America. Proc Calif Acad Sci 55:408–413

    Google Scholar 

  • Bergh R (1876) Malacologische Untersuchungen 10. In: Smeper C (ed) Reisen im Archiel der Philopponen. 2. Teil 2. Bd, pp 377–427

  • Bhave V, Apte D (2011) Illustrated checklist of Opisthobranch fauna of Ratnagiri, Maharashtra, India, with eight new records to india. J Bomb Nat Hist Soc 108:172–182

    Google Scholar 

  • Britton T, Svennblad B, Erixon P, Oxelman B (2007) Bayesian support is larger than bootstrap support in phylogenetic inference: a mathematical argument. Math Med Biol 24:401–411

    Article  PubMed  Google Scholar 

  • Brodie GD (2004) An unusual dendrodorid: redescription of the tropical nudibranch Dendrodoris atromaculata (Alder & Hancock, 1864) (Anthobranchia: Doridoidea: Dendrodorididae). Zootaxa 503:1–13

    Google Scholar 

  • Brodie GD (2005) Redescription of the Australian endemic nudibranch Dendrodoris maugeana Burn, 1962 (Gastropoda: Opisthobranchia: Doridoidea): new and reviewed features important for future phylogenetic analyses of porostomes. Mollus Res 25:37–46

    Google Scholar 

  • Brodie GD, Calado G (2006) Dendrodoris arborescens (Collingwood, 1881) (Mollusca: Nudibranchia): larval characteristics reveal a masked porostome species. Rec Aust West Mus Supl 69:119–126

    Google Scholar 

  • Brodie GD, Willan RC, Collins JD (1997) Taxonomy and occurrence of Dendrodoris nigra and Dendrodoris fumata (Nudibranchia: Dendrodorididae) in the Indo-west Pacific region. J Mol Stud 63:407–423

    Article  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Collingwood C (1881) On some new species of nudibranchiate Mollusca from the Eastern Seas. Trans Linn Soc Lond, Zool Ser 2(2):123–140

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Gohar HAF, Soliman GN (1967) The biology and development of Dendrodoris (= Doridopsis) fumata (Rüppell and Leuckart) (Gastropoda, Nudibranchia). Publ Mar Biol Sta Al-Ghardaqa, Red Sea 14:31–54

    Google Scholar 

  • Gosliner TM, Behrens DW, Valdés A (2008) Indo-pacific nudibranchs and sea slugs: a field guide to the world’s most diverse fauna. Sea Challengers/California Academy of Sciences, San Francisco

    Google Scholar 

  • Jobb G (2008) Treefinder ver. Jan 2008, Munich, Germany

  • Kelaart EF (1858) Descriptions of new and little known species of Ceylon nudibranchiate molluscs and zoophytes. J R Asiat Soc Ceylon Branch Colombo 3:84–139

    Google Scholar 

  • Krug PJ, Vendetti JE, Rodriguez AK, Retana JN, Hirano YM, Trowbridge CD (2013) Integrative species delimitation in photosynthetic sea slugs reveals twenty candidate species in three nominal taxa studied for drug discovery, plastid symbiosis or biological control. Mol Phylogenet Evol 69:1101–1119. doi:10.1016/j.ympev.2013.07.009

    Article  PubMed Central  PubMed  Google Scholar 

  • Maas AE, Blanco-Bercial L, Lawson GL (2013) Reexamination of the species assignment of Diacavolinia pteropods using DNA barcoding. PLoS ONE 8:e53889. doi:10.1371/journal.pone.0053889

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakano R (2004) Opisthobranchs of the Japanese Islands. Rutles, Inc., Tokyo (in Japanese)

    Google Scholar 

  • Nakano R (2011) Opisthobranchs (Mollusca: Gastropoda) from Nihidomari, Otsuki, Kochi Prefecture, Japan. Kuroshio Biosph 7:1–35 (in Japanese)

    Google Scholar 

  • Ohnheiser LT, Malaquias M (2013) Systematic revision of the gastropod family Philinidae (Mollusca: Cephalaspidea) in the north-east Atlantic Ocean with emphasis on the Scandinavian Peninsula. J Linn Soc-Lond 167:273–326. doi:10.1111/zoj.12000

    Article  Google Scholar 

  • Okutani T (2001) Marine mollusks in Japan. Tokai University Press, Tokyo (in Japanese)

    Google Scholar 

  • Ornelas-Gatdula E, Camacho-Garía Y, Schrödl M, Padula V, Hooker Y, Gosliner TM, Valdés A (2012) Molecular systematics of the ‘Navanax aenigmaticus’ species complex (Mollusca, Cephalaspidea): coming full circle. Zool Scr 41:374–385. doi:10.1111/j.1463-6409.2012.00538.x

    Article  Google Scholar 

  • Patel BK, Shukla ML, Apte DA (2013) First record of Dendrodoris nigra (Stimpson, 1855) from Saurashtra coast of Gujarat, India with observation on effect of sediment composition on distribution. Res J Marine Sci 1:10–14

    CAS  Google Scholar 

  • Pola M, Valles Y, Cervera JL, Medina M, Gosliner T (2006) Taxonomic status of Tambja abdere and Tambja fusca based on morphological and molecular evidence, with comments on the phylogeny of the subfamily Nembrothinae (Nudibranchia, Polyceridae). Ann Zool Fennici 43:52–64

    Google Scholar 

  • Pola M, Cervera JL, Gosliner TM (2007) Phylogenetic relationships of Nembrothinae (Mollusca: Doridacea: Polyceridae) inferred from morphology and mitochondrial DNA. Mol Phylogenet Evol 43:726–742

    Article  CAS  PubMed  Google Scholar 

  • Pola M, Camacho-Garía YE, Gosliner TM (2012) Molecular data illuminate cryptic nudibranch species: the evolution of the Scyllaeidae (Nudibranchia: Dendronotina) with a revision of Notobryon. Zool J Linn Soc-Lond 165:311–336. doi:10.1111/j.1096-3642.2012.00816.x

    Article  Google Scholar 

  • Posada D, Crandall KA (1988) Modeltest: testing the model of DNA substitution. Bioinformatics 14:814–818

    Google Scholar 

  • Rasband, WS (1997–2014) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/

  • Ronquist F, Huelsenbeck J (2003) Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rose RA (1985) The spawn and embryonic development of colour variants of Dendrodoris nigra Stimpson (Mollusca: Nudibranchia). J Malac Soc Aust 7:75–88

    Google Scholar 

  • Rüppell E, Leuckart FS (1828/1830) Mollusca. In: Atlas zu der Reise im nordlichen Afrika van Eduard Rülppell. Zoology Neue wirbellose. Thiere des Rothen Meers, 15–47

  • Sachidhanandam U, Willan RC, Chou LM (2000) Checklist of the Nudibranchs (Opisthobranchia: Nudibranchia) of the South China Sea. Raffles B Zool 8:513–537

    Google Scholar 

  • Stimpson W (1855) Descriptions of some of the new marine Invertebrata from the Chinese and Japanese Seas. Proc Acad Nat Sci Phila 7:375–384

    Google Scholar 

  • Swofford D (2003) PAUP 4.0b7a,- Phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Sunderland, Massachusetts, USA

    Google Scholar 

  • Thollesson M (2000) Increasing fidelity in parsimony analysis of dorid nudibranchs by differential weighting, or a tale of two genes. Mol Phylogenet Evol 16:161–172. doi:10.1006/mpev.2000.0789

    Article  CAS  PubMed  Google Scholar 

  • Turner LM, Wilson NG (2008) Polyphyly across oceans: a molecular phylogeny of the Chromodorididae (Mollusca, Nudibranchia). Zool Scr 37:23–42. doi:10.1111/j.1463-6409.2007.00310.x

    Google Scholar 

  • Valdés A, Ortea J, Ávila C, Ballesteros M (1996) Review of the genus Dendrodoris Ehrenberg, 1831 (Gastropoda: Nudibranchia) in the Atlantic Ocean. J Mol Stud 62:1–31

    Article  Google Scholar 

  • Wägele H, Vonnemann V, Wägele JW (2003) Towards a phylogeny of the Opisthobranchia. In: Lydeard C, Lindberg D (eds) Molecular systematics and phylogeography of mollusks. Smithsonian Institution Press, Washington, DC, pp 185–228

    Google Scholar 

  • Wilson NG, Schrödl M, Halanych KM (2009) Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Mol Ecol 18:965–984. doi:10.1111/j.1365-294X.2008.04071.x

    Article  PubMed  Google Scholar 

  • Wollscheid E, Wägele H (1999) Initial results on the molecular phylogeny of the Nudibranchia (Gastropoda, Opisthobranchia) based on 18S rDNA data. Mol Phylogenet Evol 13:215–226. doi:10.1006/mpev.1999.0664

    Article  CAS  PubMed  Google Scholar 

  • Wollscheid-Lengeling E, Boore J, Brown W, Wägele H (2001) The phylogeny of Nudibranchia (Opisthobranchia, Gastropoda, Mollusca) reconstructed by three molecular markers. Org Dibers Evol 1:241–256

    Article  Google Scholar 

  • WoRMS Editorial Board (2014). World Register of Marine Species. Available from http://www.marinespecies.org/ at VLIZ. Accessed 2014-06-25

  • Yonow N (2012) Opisthobranchs from the western Indian Ocean, with descriptions of two new species and ten new records (Mollusca, Gastropoda). Zookeys 197:1–126. doi:10.3897/zookeys.197.1728

    Article  PubMed  Google Scholar 

  • Young DK (1969) The functional morphology of the feeding apparatus of some Indo-west-Pacific dorid nudibranchs. Malacologia 9:421–445

    Google Scholar 

Download references

Acknowledgments

We thank Dr. Masami Obuchi (Biological Institute of Kuroshio, Kochi), Dr. Gen Hamanaka (Marine and Coastal Research Center, Ochanomizu University), Dr. Ryota Suwa (Seto Marine Biological Laboratory, Kyoto University), Dr. Hiroyuki Tachikawa (Natural History Museum and Institute, Chiba), Dr. Yusuke Yamana (Wakayama Prefectural Museum of Natural History), and Dr. Kensuke Yanagi (Coastal Branch of Natural History Museum and Institute, Chiba) for providing the specimens used in this study. This study was performed as a project of the Educational Cooperative-utilization Site by the Ministry of Education, Culture, Sports, Science & Technology in Japan, and partly supported by the Nippon Foundation and the International Research Hub Project for Climate Change and Coral Reef/Island Dynamics from University of the Ryukyus.

Author information

Authors and Affiliations

  1. Marine and Coastal Research Center, Ochanomizu University, Tateyama, Chiba, 294-0301, Japan

    Mamiko Hirose & Masato Kiyomoto

  2. Department of Chemistry, Biology, and Marine Science, Faculty of Science, University of the Ryukyus, Nishihara, Okinawa, 903-0213, Japan

    Euichi Hirose

Authors
  1. Mamiko Hirose
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Euichi Hirose
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masato Kiyomoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mamiko Hirose.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hirose, M., Hirose, E. & Kiyomoto, M. Identification of five species of Dendrodoris (Mollusca: Nudibranchia) from Japan, using DNA barcode and larval characters. Mar Biodiv 45, 769–780 (2015). https://doi.org/10.1007/s12526-014-0288-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-014-0288-2

Keywords

Search

Navigation