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Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
RESEARCH ARTICLE

The marine planktonic dinoflagellate Tripos: 60 years of species-level distributions in Australian waters

Gustaaf Hallegraeff https://orcid.org/0000-0001-8464-7343 A E , Ruth Eriksen B , Claire Davies B , Anita Slotwinski B , Felicity McEnnulty B , Frank Coman C , Julian Uribe-Palomino C , Mark Tonks C and Anthony Richardson C D
+ Author Affiliations
- Author Affiliations

A Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Tas. 7001, Australia.

B CSIRO Oceans and Atmosphere, Castray Esplanade, Hobart, Tas. 7000, Australia.

C CSIRO Oceans and Atmosphere, Queensland BioSciences Precinct (QBP), Saint Lucia, Qld 4072, Australia.

D Centre for Applications in Natural Resource Mathematics, School of Mathematics and Physics, The University of Queensland, Saint Lucia, Qld 4072, Australia.

E Corresponding author. Email: hallegraeff@utas.edu.au

Australian Systematic Botany 33(4) 392-411 https://doi.org/10.1071/SB19043
Submitted: 19 September 2019  Accepted: 26 March 2020   Published: 12 May 2020

Abstract

We reviewed 15 572 Australian species-level records of the marine planktonic dinoflagellate Tripos Bory (formerly Ceratium Schrank, a genus now restricted to freshwater species). The genus is represented by over 50 species and numerous varieties and forms in Australian tropical, subtropical and temperate marine waters and the Southern Ocean. There exists considerable plasticity in the morphology of many species, which has confounded species delimitations and created uncertainty around their spatial distributions. We newly illustrate by light and electron microscopy the rarely reported Tripos hundhausenii (Schröd.) Hallegr. & Huisman comb. nov. first described from the Arabian Sea, but increasingly being observed in Sydney coastal waters. A large number of Tripos species are widely distributed in temperate, subtropical and tropical waters and their distributions have remained remarkably stable in Australian waters over the past 60–80 years. By contrast, we identified a narrow group of warm-water species, including T. belone (Cleve) F.Gómez, T. cephalotus (Lemmerm.) F.Gómez, T. dens (Ostenf. & E.J.Schmidt) F.Gómez, T. digitatus (F.Schütt) F.Gómez, T. gravidus (Gourret) F.Gómez, T. incisus (G.Karst.) F.Gómez, T. paradoxides (Cleve) F.Gómez and T. praelongus (Lemmerm.) F.Gómez, that are commonly encountered off Sydney, rarely found down to Eden and Batemans Bay or Bass Strait, but occasionally occur as far south as King Island and Maria Island, Tasmania. These rare tropical Tripos species are carried southward by the East Australian and Leeuwin Currents and deserve careful attention in monitoring for future range expansions, changes in seasonality or upwelling or incursion of deep tropical waters.


References

Balech E (1976) ‘Clave Ilustrada de Dinoflagelados Antárticos. Vol. 11.’ (Publicación Instituto Antártico Argentino, Buenos Aires)

Calado A, Huisman JM (2010) Commentary: Gómez F, Moreira D, Lopez Garcia, P (2010). Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 161: 35–54. Protist 161, 517–519.
Commentary: Gómez F, Moreira D, Lopez Garcia, P (2010). Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 161: 35–54.Crossref | GoogleScholarGoogle Scholar | 20462793PubMed |

Castracane degli Antelminelli F (1886) Report on the Diatomaceae collected by HMS Challenger during the years 1873–1876. Report of the Scientific Results of the Voyage of the HMS Challenger 2(4), HMSO, London, UK.

Dakin WJ, Colefax A (1933) The marine plankton of the coastal waters of New South Wales. 1. The chief planktonic forms and their seasonal distribution. Proceedings of the Linnean Society of New South Wales 58, 186–222.

Dakin WJ, Colefax A (1940) ‘The Plankton of Australian coastal waters of New South Wales. Part 1.’ Monographs 1. (University of Sydney, Department of Zoology: Sydney, NSW, Australia)

Davies CH, Coughlan A, Hallegraeff G, Ajani P, Armbrecht L, Atkins N, Bonham P, Brett S, Brinkman R, Burford M, Clementson L, Coad P, Coman F, Davies D, Dela-Cruz J, Devlin M, Edgar S, Eriksen R, Furnas M, Hassler C, Hill D, Holmes M, Ingleton T, Jameson I, Leterme SC, Lønborg C, McLaughlin J, McEnnulty F, McKinnon AD, Miller M, Murray S, Nayar S, Patten R, Pausina SA, Pritchard T, Proctor R, Purcell-Meyerink D, Raes E, Rissik D, Ruszczyk J, Slotwinski A, Swadling KM, Tattersall K, Thompson P, Thomson P, Tonks M, Trull TW, Uribe-Palomino J, Waite AM, Yauwenas R, Zammit A, Richardson AJ (2016a) A database of marine phytoplankton abundance, biomass and species composition in Australian waters. Nature Scientific Data 3, 160043
A database of marine phytoplankton abundance, biomass and species composition in Australian waters.Crossref | GoogleScholarGoogle Scholar |

Davies CH, Coughlan A, Hallegraeff G, Ajani P, Armbrecht L, Atkins N, Bonham P, Brett S, Brinkman R, Burford M, Clementson L, Coad P, Coman F, Davies D, Dela-Cruz J, Devlin M, Edgar S, Eriksen R, Furnas M, Hassler C, Hill D, Holmes M, Ingleton T, Jameson I, Leterme SC, Lønborg C, McLaughlin J, McEnnulty F, McKinnon AD, Miller M, Murray S, Nayar S, Patten R, Pausina SA, Pritchard T, Proctor R, Purcell-Meyerink D, Raes E, Rissik D, Ruszczyk J, Slotwinski A, Swadling KM, Tattersall K, Thompson P, Thomson P, Tonks M, Trull TW, Uribe-Palomino J, Waite AM, Yauwenas R, Zammit A, Richardson AJ (2016b) Corrigendum: a database of marine phytoplankton abundance, biomass and species composition in Australian waters. Nature Scientific Data 3, 160111
Corrigendum: a database of marine phytoplankton abundance, biomass and species composition in Australian waters.Crossref | GoogleScholarGoogle Scholar |

Dodge JD, Marshall HG (1994) Biogeographic analysis of the armored plankton dinoflagellate Ceratium in the North Atlantic and adjacent seas. Journal of Phycology 30, 905–922.
Biogeographic analysis of the armored plankton dinoflagellate Ceratium in the North Atlantic and adjacent seas.Crossref | GoogleScholarGoogle Scholar |

Eriksen RS, Davies CH, Bonham P, Coman FE, Edgar S, McEnnulty F, McLeod D, Miller MJ, Rochester W, Slotwinski A, Tonks ML, Uribe-Palomino J, Richardson AJ (2019) Australia’s long-term plankton observations: the Integrated Marine Observing System National Reference Station network. Frontiers in Marine Science 6, 161
Australia’s long-term plankton observations: the Integrated Marine Observing System National Reference Station network.Crossref | GoogleScholarGoogle Scholar |

Gómez F (2013) Reinstatement of the dinoflagellate genus Tripos to replace Neoceratium, marine species of Ceratium (Dinophyceae, Alveolata). CICIMAR Oceánides 28, 1–22.

Gómez F, Moreira D, López-García P (2010) Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 161, 35–54.
Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae).Crossref | GoogleScholarGoogle Scholar | 19665427PubMed |

Graham HW, Bronikovsky N (1944) The genus Ceratium in the Pacific and North Atlantic Oceans. Carnegie Institute of Washington Publication 565, 1–09.

Hallegraeff GM, Jeffrey SW (1984) Tropical phytoplankton species and pigments in continental shelf waters of North and North-West Australia Marine Ecology Progress Series 20, 59–74.
Tropical phytoplankton species and pigments in continental shelf waters of North and North-West AustraliaCrossref | GoogleScholarGoogle Scholar |

Hallegraeff GM, Reid DD (1986) Phytoplankton species successions and their hydrological environment at a coastal station off Sydney. Australian Journal of Marine and Freshwater Research 37, 361–377.
Phytoplankton species successions and their hydrological environment at a coastal station off Sydney.Crossref | GoogleScholarGoogle Scholar |

Hallegraeff GM, Bolch CJS, Hill DRA, Jameson I, Leroi J-M, McMinn A, Murray S, De Salas MF, Saunders K (Eds) (2010) ‘Algae of Australia: Phytoplankton of Temperate Coastal Waters.’ (ABRS: Canberra, ACT, Australia; and CSIRO Publishing: Melbourne, Vic., Australia.)

Heron AC (1982) A vertical free fall plankton net with no mouth obstructions. Limnology and Oceanography 27, 380–383.
A vertical free fall plankton net with no mouth obstructions.Crossref | GoogleScholarGoogle Scholar |

Huisman JM (1989) The genus Ceratium Schrank (Dinophyceae) in Bass Strait and adjoining waters, southern Australia. Australian Systematic Botany 2, 425–454.
The genus Ceratium Schrank (Dinophyceae) in Bass Strait and adjoining waters, southern Australia.Crossref | GoogleScholarGoogle Scholar |

Jeffrey SW, Hallegraeff GM (1987) Phytoplankton pigments, species and light climate in a complex warm-core eddy (Mario) of the East Australian Current. Deep-Sea Research 34, 649–673.
Phytoplankton pigments, species and light climate in a complex warm-core eddy (Mario) of the East Australian Current.Crossref | GoogleScholarGoogle Scholar |

Jörgensen E (1920) Mediterranean Ceratia. Report on the Danish Oceanographical Expeditions 1908–10 to the Mediterranean and adjacent Seas 2 (Biology) J1, Carlsbergfondet, Copenhagen, Denmark.

McDermott G, Raine RC (2006) ‘The Dinoflagellate Genus Ceratium in Irish Shelf Seas.’ (The Martin Ryan Institute, National University of Ireland: Galway, Ireland)

Omura T, Iwataki M, Borja VM, Takayama H, Fukuyo Y (2012) ‘Marine Phytoplankton of the Western Pacific.’ (Kouseisha Kouseikaku: Tokyo, Japan)

Pizay M-D, Lemee R, Simon N, Cras A-L, Laugier J-P, Dolan JR (2009) Night and day morphologies in a planktonic dinoflagellate Protist 160, 565–575.
Night and day morphologies in a planktonic dinoflagellateCrossref | GoogleScholarGoogle Scholar | 19577958PubMed |

Richardson AJ, Walne AW, John AWG, Jonas TD, Lindley JA, Sims DW, Stevens D, Witt M (2006) Using continuous plankton recorder data. Progress in Oceanography 68, 27–74.
Using continuous plankton recorder data.Crossref | GoogleScholarGoogle Scholar |

Schröder B (1906) Beitrage zur Kenntnis des Phytoplanktons warmer Meere. Vierteljahrsschrift der Naturforschenden Gesellschaft in Zürich 51, 319–377.

Scott FJ, Marchant HJ (Eds) (2005) ‘Antarctic Marine Protists.’ (ABRS and Australian Antarctic Division: Hobart, Tas., Australia)

Sournia A (1967) Le genre Ceratium (péridinien planctonique) dans le Canal de Mozambique: contribution à une révision mondiale. Vie Milieu A 18, 375–499.

Sournia A (1982) Is there a shade flora in the marine plankton? Journal of Plankton Research 4, 391–399.
Is there a shade flora in the marine plankton?Crossref | GoogleScholarGoogle Scholar |

Taylor FJR (1976) Dinoflagellates from the International Indian Ocean Expedition. A report on material collected by the R.V. ‘Anton Bruun’ 1963–1964. Bibliotheca Botanica 132, 1–234.

Tunin-Ley A, Ibanez F, Labat JP, Zingone A, Lemée R (2009) Phytoplankton biodiversity and climate change in NW Mediterranean Sea: changes in dinoflagellate genus Ceratium over the last century. Marine Ecology Progress Series 375, 85–99.
Phytoplankton biodiversity and climate change in NW Mediterranean Sea: changes in dinoflagellate genus Ceratium over the last century.Crossref | GoogleScholarGoogle Scholar |

Turland NJ, Wiersema JH, Barrie FR, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Kusber W-H, Li D-Z, Marhold K, May TW, McNeill J, Monro AM, Prado J, Price MJ, Smith GF (Eds) (2018) ‘International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. (Koeltz Botanical Books: Glashütten, Germany.) 10.12705/Code.2018 10.12705/Code.2018

Wood EJF (1954) Dinoflagellates in the Australian region. Australian Journal of Marine and Freshwater Research 5, 171–351.
Dinoflagellates in the Australian region.Crossref | GoogleScholarGoogle Scholar |

Wood EJF (1963) Dinoflagellates in the Australian region. II. Recent collections. Oceanography technical paper 14, CSIRO Division Fisheries, Sydney, NSW, Australia.