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Morphological and molecular diagnostic species characters of Staurozoa (Cnidaria) collected on the coast of Helgoland (German Bight, North Sea)

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Abstract

Scientific knowledge and records on staurozoans are limited probably because of their inconspicuous life habit and the small number of specialists for this taxon. To increase the awareness for Staurozoa, we identified morphological and molecular features of the three staurozoan species Haliclystus tenuis Kishinouye, 1910, Haliclystus auricula Clark, 1863, and Craterolophus convolvulus (Johnston, 1835) collected on the coast of the island Helgoland to evaluate their suitability as diagnostic characters. Useful macromorphological diagnostic features were the patterns of white spots of nematocysts and internal arm structures, whereas tentacle and gonad follicle numbers showed high intraspecific variations. Morphometric measurements on photographs of living specimens provided reliable data for interspecific comparisons. Comprehensive nematocyst analyses revealed interspecific shape differences of isorhizas and three types of rhopaloids, indicating that the staurozoan cnidome is more diverse than previously assumed. However, the taxonomic value of nematocyst analyses in Staurozoa remains unclear because comprehensive data is still lacking for most species. Comparative molecular genetic sequence analyses of mitochondrial 16S and cytochrome c oxidase subunit I (COI) and nuclear 18S ribosomal DNA identified the three species and confirmed their morphological identification. In comparison to published data, our analyses indicate similarities between H. auricula and Haliclystus antarcticus Pfeffer, 1889. Proteomic fingerprinting by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) differentiated all three species, suggesting that this technique could provide an alternative rapid identification method for staurozoans.

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Acknowledgements

We thank Karen Jeskulke for her assistance in sampling and laboratory work. We gratefully appreciate the scientific guest research service provided by the Biological Institute Helgoland (BAH) of the Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research. We thank Thomas Glatzel (Carl von Ossietzky University of Oldenburg) for the collaboration. This is publication no. 6 of Senckenberg am Meer Proteome Laboratory and publication no. 59 of Senckenberg am Meer Metabarcoding and Molecular Laboratory.

Funding

This study was funded by the Federal Ministry of Education and Research of Germany (BMBF Grant Nos. 03F0499A and 03F0664A) and the Land Niedersachsen.

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Author notes

  1. Silke Laakmann

    Present address: Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg (HIFMB), Ammerländer Heerstraße 231, 26129, Oldenburg, Germany

Authors and Affiliations

  1. German Center for Marine Biodiversity Research, Senckenberg am Meer, Martin-Luther-King-Platz 3, 20146, Hamburg, Germany

    Sabine Holst

  2. Research Group Animal Biodiversity and Evolutionary Biology, Institute for Biology and Environmental Sciences, Carl von Ossietzky University of Oldenburg, Carl-von-Ossietzky-Straße 9-11, 26129, Oldenburg, Germany

    Anneke Heins

  3. German Center for Marine Biodiversity Research, Senckenberg am Meer, Suedstrand 44, 26382, Wilhelmshaven, Germany

    Silke Laakmann

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  1. Sabine Holst
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Correspondence to Sabine Holst.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.

Data availability

Genetic sequence data generated in this study were deposited in GenBank with Accession Numbers MF322725–MF322746 and MF346293–MF346312. For all three gene fragments (COI, 16S and 18S rDNA), the multiple alignments, NJ and ML trees are available in Ddryad digital repository (https://doi.org/10.5061/dryad.5cr6008). Raw data on nematocyst measurements and proteomic mass spectra analyzed during the current study are available from the corresponding author on reasonable request.

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Communicated by S. Piraino

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Electronic supplementary material

Online Resource 1

Body parts used for nematocyst analyses. GF gastric filaments, ST secondary tentacle knobs, AN/PT anchors/primary tentacles, EP exumbrella perradial, EI exumbrella interradial, SP subumbrella perradial, SI subumbrella interradial (DOCX 19 kb)

Online Resource 2

Sequences from GenBank and from own studies used for molecular genetic analyses (Neighbour Joining and Maximum Likelihood analyses) (DOCX 28 kb)

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Test statistics of parameters compared among species. ANOVA Kruskal-Wallis one-way analysis of variance on ranks, Cc Craterolophus convolvulus, Ha Haliclystus auricula, Ht Haliclystus tenuis, Iso isorhiza, Nc nematocyst, R1 rhopaloid type 1, R2 rhopaloid type 2, R3 rhopaloid type 3, Rank sum Mann-Whitney rank sum test (DOCX 19 kb)

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Holst, S., Heins, A. & Laakmann, S. Morphological and molecular diagnostic species characters of Staurozoa (Cnidaria) collected on the coast of Helgoland (German Bight, North Sea). Mar Biodiv 49, 1775–1797 (2019). https://doi.org/10.1007/s12526-019-00943-1

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  • DOI: https://doi.org/10.1007/s12526-019-00943-1

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