Skip to main content
Log in

Morphological and molecular investigations of the rhizocephalan barnacle Peltogaster lineata Shiino, 1943 in the northern part of the species range (Peter the Great Bay, the Sea of Japan)

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

Abstract

A parasitic rhizocephalan barnacle Peltogaster lineata Shiino, 1943 (Cirripedia, Rhizocephala, Peltogastridae) was found in Vostok Bay (Peter the Great Bay, the northwestern Sea of Japan), on young specimens of the hermit crab Pagurus brachiomastus (Thallwitz, 1891). This rhizocephalan was described using molecular and morphological methods. The reproductive organs were investigated by histological methods. Cuticle was visualized using SEM. Peltogaster lineata from Japanese, Korean, and Russian waters turned out to be very similar by the molecular markers and by the morphology of the externa. Peltogaster lineata differs from Peltogaster reticulata Shiino, 1943 occurring in Russian waters by the molecular markers, the shape and color of the externa, the shape of the retinacula, and the length of the receptacle ducts. Hyperparasitic isopod Liriopsis pygmaea (Rathke, 1843) was found in the externa of P. lineata for the first time. The host preference of P. lineata was changing from Pagurus filholi + Pagurus nigrivittatus + Pagurus maculosus in Japan to P. filholi + P. brachiomastus in Korea and to only P. brachiomastus in Russia. At present, Peter the Great Bay is the northern border of the distribution range of P. lineata.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Alasaad S, Rossi L, Maione S, Sartore S, Soriguer RC, Pérez JM, Rasero R, Zhu XQ, Soglia D (2008) HotSHOT Plus ThermalSHOCK, a new and efficient technique for preparation of PCR-quality mite genomic DNA. Parasitol Res 103:1455. https://doi.org/10.1007/s00436-008-1127-9

    Article  CAS  PubMed  Google Scholar 

  • Boschma H (1927) On the larval forms of Rhizocephala. Proc Sect Sci Koninklijke Akademie Van Wetenschappen Te Amsterdam 30:293–297

    Google Scholar 

  • Boschma H (1930) Briarosaccus callosus, a new genus and new species of a rhizocephalan parasite of Lithodes agassizii Smith. Proc US Nat Mus 76(7):1–8

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duboscq O (1912) Sur les peltogastrides des cotes de France Peltogaster (Chlorogaster) pruvoti n. sp., Peltogaster (Chlorogaster) delagei n. sp., Septosaccus cuenoti n. g., n. sp. Archives de Zoologie Expérimentale et Générale, 5th sér. 9

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  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(5):294–299

    CAS  PubMed  Google Scholar 

  • Fraisse P (1878) Die gattung Cryptoniscus Fr. Müller (Liriope Rathke). Arbeiten aus dem Zoologisch-Zootomischen Institut in Würzburg 4(3):239–296

  • Golubinskaya DD, Korn OM, Sharina SN, Selin NI (2021) Sympatric two-species infestation by rhizocephalan barnacle parasites in the spider crab Pugettia aff. ferox Ohtsuchi & Kawamura, 2019 from Peter the Great Bay (Northwestern Sea of Japan). Zool Stud 60:54. https://doi.org/10.6620/ZS.2021.60-54

    Article  Google Scholar 

  • Høeg JT, Noever C, Rees DJ, Crandall KA, Glenner H (2020) A new molecular phylogeny-based taxonomy of the parasitic barnacles (Crustacea: Cirripedia: Rhizocephala). Zool J Linn Soc 190(2):632–653. https://doi.org/10.1093/zoolinnean/zlz140

    Article  Google Scholar 

  • Jung J, Yoshida R, Kim W (2019) Diversity of parasitic peltogastrid barnacles (Crustacea: Cirripedia: Rhizocephala) on hermit crabs in Korea. Zool Stud 58:33. https://doi.org/10.6620/ZS.2019.58-33

    Article  Google Scholar 

  • Kappner I, Bieler R (2006) Phylogeny of venus clams (Bivalvia: Venerinae) as inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol 40(2):317–331. https://doi.org/10.1016/j.ympev.2006.02.006

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolution aryrates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581

    Article  CAS  PubMed  Google Scholar 

  • Komai T (2000) The identity of Pagurus brachiomastus and descriptions of two new species of Pagurus (Crustacea: Decapoda: Anomura: Paguridae) from the northwestern Pacific. Species Diversity 5:229–265. https://doi.org/10.12782/specdiv.5.229

  • Korn OM, Golubinskaya DD, Rees DJ, Glenner H, Høeg JT (2020a) Phylogenetic position, complete larval development and larval sexual dimorphism in a rhizocephalan barnacle, Lernaeodiscus rybakovi sp. nov. (Cirripedia: Rhizocephala: Peltogastridae), parasitizing the crab Pachycheles stevensii Stimpson, 1858 (Decapoda: Anomura: Porcellanidae). Zool Anz 287:178–197. https://doi.org/10.1016/j.jcz.2020.06.005

    Article  Google Scholar 

  • Korn OM, Golubinskaya DD, Sharina SN (2020b). The parasitic barnacle Peltogaster reticulata Shiino, 1943 (Rhizocephala, Peltogastridae) from Russian waters of the Sea of Japan: morphological description, molecular identification and complete larval development. Zootaxa 4768(1):006–024. https://doi.org/10.11646/zootaxa.4768.1.2

  • Korn OM, Kornienko ES, Selin NI (2018) Population biology and reproductive characteristics of the hermit crab Pagurus minutus Hess, 1865 (Decapoda: Anomura: Paguridae) in the northern part of the species range (Peter the Great Bay, the Sea of Japan). Mar Biol Res 14(8):846–855. https://doi.org/10.1080/17451000.2018.1503685

    Article  Google Scholar 

  • Korn OM, Shukalyuk AI, Trofimova AV, Isaeva VV (2004) Reproductive stage of the life cycle in the rhizocephalan barnacle Polyascus polygenea (Crustacea: Cirripedia). Russ J Mar Biol 30(5):328–340

    Article  Google Scholar 

  • Kornienko ES, Korn OM, Selin NI (2018) The parasitic fauna of common species of hermit crabs of Vostok Bay (Sea of Japan). Russ J Mar Biol 44(2):94–99. https://doi.org/10.1134/S1063074018020062

    Article  Google Scholar 

  • Kornienko EC, Selin NI, Korn OM (2017) Population and reproductive characteristics of the hermit crab Pagurus proximus Komai, 2000 (Decapoda: Anomura: Paguridae) in the northern part of the species range. J Mar Biol Assoc U K 99(1):101–109. https://doi.org/10.1017/S0025315417001679

    Article  Google Scholar 

  • Kornienko EC, Selin NI (2019) The population and reproductive characteristics of the hermit crab Pagurus brachiomastus (Thallwitz, 1892) (Decapoda: Paguridae) from Peter the Great Bay, the Sea of Japan. Russ J Mar Biol 45(3):174–184. https://doi.org/10.1134/S1063074019030088

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lilljeborg W (1861) Supplément au mémoire sur les genres Liriope et Peltogaster, H. Rathke. Nova Acta Regiae Societatis Scientiarum Upsaliensis, Seriei Tertiae 3:74–102

    Google Scholar 

  • Marin IN (2013) Atlas of Decapod Crustaceans of Russia. KMK Scientific Press, Moscow (in Russian, with English abstract)

  • McDermott JJ, Williams JD, Boyko CB (2010) The unwanted guests of hermits: a global review of the diversity and natural history of hermit crab parasites. J Exp Mar Biol Ecol 394:2–44. https://doi.org/10.1016/j.jembe.2010.06.022

    Article  Google Scholar 

  • Meyer CP (2003) Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biol J Linnean Soc 79:401–459. https://doi.org/10.1046/j.1095-8312.2003.00197.x

    Article  Google Scholar 

  • Meyer CP, Paulay G (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biol 3(12):e422. https://doi.org/10.1371/journal.pbio.0030422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, Louisiana, 14 Nov 2010. IEEE, New York. https://doi.org/10.1109/GCE.2010.5676129

  • Morgulis M, Coulouris G, Rayselis Y, Madden TL, Agarwala R, Schäffer AA (2008) Database indexing for production Mega BLAST searches. Bioinformatics 24(16):1757–1764. https://doi.org/10.1093/bioinformatics/btn322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller F (1862) Die Rhizocephalen, eine neue Gruppe schmarotzender Kruster. Archiv Für Naturgeschichte 28:1–9

    Google Scholar 

  • Peresan L, Roccatagliata D (2005) First record of the hyperparasite Liriopsis pygmaea (Cryptoniscidae, Isopoda) from a rhizocephalan parasite of the false king crab Paralomis granulosa from thr Beagle Channel (Argentina), with a redescription. J Nat Hist 39(4):311–324. https://doi.org/10.1080/0022293042000200103

    Article  Google Scholar 

  • Rathke H (1842) Beiträge zur vergleichenden Anatomie und Physiologie, Reisebemerkungen aus Skandinavien, nebst einem Anhange über die rückschreitende Metamorphose der Thiere. Nueste Schriften Der Naturforschenden Gesellschaft in Danzing 3:1–162

    Google Scholar 

  • Rathke H (1843) Beiträge zur Fauna Norwegens. Nova Acta Academiae Caesareae Leopoldino-Carolinae Naturae Curiosorum, Breslau & Bonn 20:1–264. https://doi.org/10.5962/bhl.title.11613

    Article  Google Scholar 

  • Reinhard EG (1944) Rhizocephalan parasites of hermit crabs from the northwest Pacific. J Wash Acad Sci 34:49–58

    Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Rybakov AV, Høeg JT (2002) The ultrastructure of retinacula in the Rhizocephala (Crustacea:Cirripedia) and their systematic significance. Zool Anz 241:95–103. https://doi.org/10.1078/0044-5231-00023

    Article  Google Scholar 

  • Shiino SM (1943) Rhizocephala of Japan. J Sigenkagaku Kenkyusyo 1(1):1–36

    Google Scholar 

  • Thallwitz J (1891) Decapoden-Studien, insbesondere basirt auf A.B. Meyer’s Sammlungen im Ostindischen Archipel, nebst einer Aufzählung der Decapoden und Stomatopoden des Dresdener Museums. Abhandlungen und Berichte des Königlichen Zoologischen und Anthropologisch–Etnographischen Museums zu Dresden 3 (3):1–56

  • Tudge CC, Asakura A, Ahyong ST (2012) Infraorder Anomura MacLeay, 1838. In: Schram FR and von Vaupel Klein JC (eds) The Crustacea, 9(B), Brill, Leiden, pp 221–333

  • Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27:171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x

    Article  PubMed  Google Scholar 

  • Warrenchuk JJ, Shirley TC (2000) Parasitism by the rhizocephalan Peltogaster paguri Rathke, 1842 and hyperparasitism by the bopyrid isopod Liriopsis pygmaea (Rathke, 1843) on Pagurus hirsutiusculus (Dana, 1851) in southeastern Alaska. Crustaceana 73(8):971–977

    Article  Google Scholar 

  • Yoshida R, Hirose M, Mok H-K, Hirose E (2012) The first records of peltogastrid rhizocephalans (Crustacea: Cirripedia: Rhizocephala) on hermit crabs (Paguroidea) in Taiwan and differences in prevalences among collection sites. Zool Stud 51(7):1027–1039

    Google Scholar 

  • Yoshida R, Hirose M, Hirose E (2014) Hermit crab host prevalence by species of Peltogastridae (Cirripedia: Rhizocephala): hosts vary with locations on the Pacific coast in mainland Japan. J Crustac Biol 34(4):467–480. https://doi.org/10.1163/1937240X-00002246

    Article  Google Scholar 

  • Yoshida R, Naruse T (2016) A new species of the genus Peltogaster Rathke, 1842 (Cirripedia: Rhizocephala: Peltogastridae) parasitizing the hermit crab Pagurixus boninensis (Melin, 1939) from the Bonin Islands, Japan. Zootaxa 4139(2):209–220 https://doi.org/10.11646/zootaxa.4139.2.5

  • Yoshida R, Osawa M, Hirose M, Hirose E (2011) A new genus and two new species of Peltogastridae (Crustacea: Cirripedia: Rhizocephala) parasitizing hermit crabs from Okinawa Island (Ryukyu Archipelago, Japan), and their DNA-barcodes. Zool Sci 28(11):853–862. https://doi.org/10.2108/zsj.28.853

    Article  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2004) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214. https://doi.org/10.1089/10665270050081478

    Article  Google Scholar 

  • Zharkikh A, Li W-H (1995) Estimation of confidence in phylogeny: the complete-and-partial bootstrap technique. Mol Phylogenet Evol 4(1):44–63. https://doi.org/10.1006/mpev.1995.1005

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Denis V. Fomin for the technical assistance with facilities of the Far Eastern Center of Electron Microscopy (A.V. Zhirmunsky National Scientific Center of Marine Biology, FEB RAS, Vladivostok, Russia). We are also greatly indebted to anonymous reviewers whose comments allowed to improve our manuscript.

Funding

The report study was funded by RFBR, project number 20–04-00097.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Darya D. Golubinskaya.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on request.

Author contribution

OMK and DDG studied morphological characters. SNS performed the molecular analysis. AAM performed the histology. OMK wrote the manuscript. DDG performed all illustrations. All authors read and approved the manuscript.

Additional information

Communicated by E. Macpherson

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.

Supplementary file1 (PDF 706 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Golubinskaya, D.D., Korn, O.M., Sharina, S.N. et al. Morphological and molecular investigations of the rhizocephalan barnacle Peltogaster lineata Shiino, 1943 in the northern part of the species range (Peter the Great Bay, the Sea of Japan). Mar. Biodivers. 51, 96 (2021). https://doi.org/10.1007/s12526-021-01239-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12526-021-01239-z

Keywords

Navigation