Detection of Prorocentrum shikokuense in the Mediterranean Sea and evidence that P. dentatum, P. obtusidens and P. shikokuense are three different species (Prorocentrales, Dinophyceae)

Fernando Gómez; Huan  Zhang; Leonilde  Roselli; Senjie  Lin

Detection of Prorocentrum shikokuense in the Mediterranean Sea and evidence that P. dentatum, P. obtusidens and P. shikokuense are three different species (Prorocentrales, Dinophyceae)

Publication date: 14.02.2022

Acta Protozoologica, 2021, Volume 60, pp. 47 - 59

https://doi.org/10.4467/16890027AP.21.006.15380

Authors

Pobierz pełny tekst

PDF

Titles

Detection of Prorocentrum shikokuense in the Mediterranean Sea and evidence that P. dentatum, P. obtusidens and P. shikokuense are three different species (Prorocentrales, Dinophyceae)

Abstract

A dinoflagellate identified as Prorocentrum dentatum, P. shikokuense or P. donghaiense is responsible of massive harmful events. Blooms of a species identified as P. shikokuense have been recently reported in the Mediterranean Sea, and an exotic origin, tentatively introduced by ballast waters from Asia, has been hypothesized. The molecular data based on the small-, large subunit, and internal transcriber spacers ribosomal RNA gene (SSU-, LSU-, ITS rRNA) sequences confirmed P. shikokuense in the Mediterranean Sea. The Mediterranean ribotype is identical to a subtropical North Atlantic ribotype, and with slight divergence from the numerous sequences from the Pacific Ocean. To revisit the relationship between P. shikokuense (=P. donghaiense) and P. obtusidens, we provide the first micrographs of P. dentatum and P. obtusidens, the latter collected from the type locality. Our observations indicate that P. dentatum, P. obtusidens, and P. shikokuense are three different species. Their diagnostic morphological characters are: Prorocentrum dentatum is 44–60 μm long, leaf-shaped, pointed and central posterior end, conspicuous anterior shoulder; P. obtusidens is 33–41 μm long, irregular parallelepiped, almost paralel valve margins, eccentric and pointed posterior end, moderate anterior shoulder; and P. shikokuense is 25 μm long, sunflower seed-shaped, round and centric posterior end, inconspicuous anterior shoulder.

Keywords

Dinophyta, harmful algae bloom, invasive alien species, non-indigenous species, molecular phylogenetics, toxic phytoplankton

References

Download references

Böhm A. (1936) Dinoflagellates of the coastal waters of the western Pacific. Bernice P. Bishop Mus. Bull. 137: 1–54

Bursa A. (1959) The genus Prorocentrum Ehrenberg. Morphodynamics, protoplasmatic structures and taxonomy. Can. J. Bot. 37: 1−31

Dodge J. D. (1975) The Prorocentrales (Dinophyceae). II. Revision of the taxonomy within the genus Prorocentrum. Bot. J. Linn. Soc. 71: 103–125

Fukuyo Y., Takano H., Chihara M. and Matsuoka K. (1990) Red tide organisms in Japan, an illustrated taxonomic guide. Uchida Rokakuho, Tokyo

Gómez F. and Furuya K. (2007) Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. Eur. J. Protistol. 43: 115–124

Gómez F., Claustre H. and Souissi S. (2008) Rarely reported dinoflagellates of the genera Ceratium, Gloeodinium, Histioneis, Oxytoxum and Prorocentrum (Dinophyceae) from the open southeast Pacific Ocean. Rev. Biol. Mar. Oceanogr. 43: 25–40

Gómez F., Qiu D. and Lin S. (2017) The synonymy of the toxic dinoflagellates Prorocentrum mexicanum and P. rhathymum and the description of P. steidingerae sp. nov. (Prorocentrales, Dinophyceae). J. Eukaryot. Microbiol. 64: 668–677

Gómez F. and Galil B. (2021) Comments on the “Mediterranean alien harmful algal blooms” by Marampouti et al. Environ. Sci. Pollut. Res. 28: 58810–58811

Hada Y. (1975) On two new species of the genus Prorocentrum Ehrenberg belonging to Dinoflagellida. Hiroshima Shudo Daigaku Ronshu 16: 31–38

Hernández-Becerril D. U., Altamirano, R. C. and Alonso, R. R. (2000) The dinoflagellate genus Prorocentrum along the coasts of the Mexican Pacific. Hydrobiologia 418: 111–121

Kumar S., Stecher G. and Tamura K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874

Lohmann H. (1920) Die Bevölkerung des Ozeans mit Plankton nach den Ergebnissen der Zentrigugenfänge während der Ausreise der “Deutschland” 1911. Zugleich ein Beitrag zur Biologie des Atlantischen Ozeans. Arch. Biontologie 4: 1–617

Lu D. and Goebel J. (2001) Five red tide species in genus Prorocentrum including the description of Prorocentrum donghaiense Lu sp. nov. from the East China Sea. Chin. J. Oceanol. Limnol. 19: 337–344

Lu D., Goebel J., Qi Y., Zou J., Han X., Gao Y. and Li Y. (2005) Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae 4: 493–505

Madhu N. V., Anil P., Gireeshkumar T. R., Muraleedharan K. R., Kiran K. and Vishal C. R. (2020) Phytoplankton characterisation in the Alappuzha mud banks during the pre-/post phases of a red-tide, Prorocentrum shikokuense Hada. Reg. Stud. Mar. Sci. 40: 101486

Marampouti C., Buma A. G. J. and de Boer, M. K. (2021) Mediterranean alien harmful algal blooms: origins and impacts. Environ. Sci. Pollut. Res. 28: 3837–3851

Margalef R. (1973) Fitoplancton marino de la región de afloramiento del NW de África. II. Composición y distribución del fitoplancton. Res. Exped. Cient. Buque Oceanográfico Cornide de Saavedra 2: 65–94

Monti-Birkenmeier M., Berden Zrimec M., Drinovec L., Beran A., Zrimec A., Cataletto B. and Fonda Umani S. (2019) Influence of salinity on growth and cell volume in three strains of Prorocentrum cordatum (Dinophyceae). Aquat. Biol. 28: 1–12

Parke M. and Ballantine D. (1957) A new marine dinoflagellate Exuviaella mariae-lebouriae n. sp. J. Mar. Biol. Assoc. U.K. 36: 643−650

Percopo I., Siano R., Cerino F., Sarno D. and Zingone A. (2011) Phytoplankton diversity during the spring bloom in the northwestern Mediterranean Sea. Bot. Mar. 54: 243–267

Pertola S., Faust M. A., Kuosa H. and Hällfors G. (2003) Morphology of Prorocentrum minimum (Dinophyceae) in the Baltic Sea and in Chesapeake Bay: comparison of cell shapes and thecal ornamentation. Bot. Mar. 46: 477–486

Rampi L. (1969) Péridiniens, Heterococcales et Pterospermales rares, intéressants ou nouveaux récoltes dans la mer Ligurienne (Méditerranée Occidentale). Natura Milano 60: 313–333

Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., Larget B., Liu L., Suchard M. A. and Huelsenbeck J. P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542

Roselli L., Vadrucci M. R., Fanelli F., Ungaro N. and Caroppo C. (2019) First bloom event of the small dinoflagellate Prorocentrum shikokuense in the Mediterranean Sea: cryptogenic of introduced? Mar. Pollut. Bull. 139: 197–204

Schiller J. (1918) Uber neue Prorocentrum und Exuviaella Arten aus der Adria. Arch. Protistenk. 38: 250–262

Schiller J. (1928) Die planktischen Vegetationen des adriatischen Meeres. C. Dinoflagellata. 1 Teil. Adiniferidea, Dinophysidaceae. Arch. Protistenk. 61: 45–91

Schiller J. (1931) Dinoflagellatae (Peridineae). In: Dr. L Rabenhosrst’s Kryptogamen-Flora von Deutschland, Österreich und der schweiz (Ed. R. Kolkwitz). 2. Aufl. 10. Bd 3. Abt. 1 Teil. Akademische Verlags., Leipzig, 1–256

Shin H. H., Li A., Mertens K. N., Seo M. H., Gu H., Lim W. A., Yoon Y. H., Soh H. Y. and Matsuoka K. (2019) Prorocentrum shikokuense Hada and P. donghaiense Lu are junior synonyms of P. obtusidens Schiller, but not of P. dentatum Stein (Prorocentrales, Dinophyceae). Harmful Algae 89: 101686

Stein F. (1883) Der Organismus der Infusionsthiere nach eigenen forschungen in systematischere Reihenfolge bearbeitet. III. Abtheilung. II. Hälfte die Naturgeschichte der Arthrodelen Flagellaten. W. Engelmann, Leipzig, Germany

Su-Myat and Koike K. (2013) A red tide off the Myanmar coast: Morphological and genetic identification of the dinoflagellate composition. Harmful Algae 27: 149–158

Takano Y. and Matsuoka K. (2011) A comparative study between Prorocentrum shikokuense and P. donghaiense (Prorocentrales, Dinophyceae) based on morphology and DNA sequences. Plankton Benthos Res. 6: 179–186

Wang L., Zhuang Y., Zhang H., Lin X. and Lin S. (2014) DNA barcoding species in Alexandrium tamarense complex using ITS and proposing designation of five species. Harmful Algae 31: 100–113

Wood E. J. F. (1963) Dinoflagellates in the Australian region. III. Further collections. Tech. Pap. Div. Fish. Oceanogr. 17: 1–20

Zhang H. and Lin S. (2005) Development of a cob-18S rRNA gene real-time PCR assay for quantifying Pfiesteria shumwayae in the natural environment. Appl. Environ. Microbiol. 71: 7053–7063

Zhang H., Bhattacharya D. and Lin S. (2005) Phylogeny of dinoflagellates based on mitochondrial cytochrome B and nuclear small subunit rDNA sequence comparisons. J. Phycol. 41: 411–420

Information

Information: Acta Protozoologica, 2021, Volume 60, pp. 47 - 59

DOI: https://doi.org/10.4467/16890027AP.21.006.15380

Article type: Original article

Authors

Fernando Gómez

Université du Littoral Côte d’Opale, Université de Lille, CNRS UMR 8187 LOG, Laboratoire d’Océanologie et de Géosciences, Maison de la Recherche en Environnement Naturel, 32 av. Foch, 62930 Wimereux, France

Carmen Campos Panisse 3, E-11500 Puerto de Santa María, Spain

Huan Zhang

Department of Marine Sciences, University of Connecticut, Groton, CT 06340, USA

Leonilde Roselli

CNR-IRET National Research Council - Research Institute on Terrestrial Ecosystems, Via P. Castellino 11, 80131 Napoli, Italy

Senjie Lin

Department of Marine Sciences, University of Connecticut, Groton, CT 06340, USA

Published at: 14.02.2022

Received at: 08.11.2021

Accepted at: 26.01.2022

Article status: Open

Licence: CC BY

Article financing:

Observations in the Pacific Ocean were supported by the European Commission [grant ICB2-CT-2001-80002]. Sampling in the port of Brindisi was supported by the Italian Ministero dell’Ambiente e della Tutela del Territorio e del Mare in order to fullfil the EU Marine Strategy Framework Directive. We thank the project Remedia [grant LIFE16ENV/IT/000343] for the sample collected at Taranto.

Percentage share of authors:

Fernando Gómez (Author) - 25%

Huan Zhang (Author) - 25%

Leonilde Roselli (Author) - 25%

Senjie Lin (Author) - 25%

Article corrections:

Publication languages:

English

View count: 751

Number of downloads: 653

Detection of Prorocentrum shikokuense in the Mediterranean Sea and evidence that P. dentatum, P. obtusidens and P. shikokuense are three different species (Prorocentrales, Dinophyceae)

Download xml