Harmful Australian Marine Microalgae

By Gustaaf M. Hallegraeff

Algal blooms have the potential to wipe out fish farms virtually overnight. Contamination of seafoods with algal toxins can poison human consumers of fish and shellfish. During the past two decades, globally there have been significant increases in economic loss and human health impact due to harmful algal blooms.

Harmful Australian Marine Microalgae offers fish and shellfish farmers information on how to effectively identify and monitor for the presence of algal species and take the appropriate species-specific countermeasures. Species descriptions are accompanied by a summary of the known distribution of the alga, its toxicology and, where available, suggestions for countermeasures. The book includes line drawings, light micrographs and electron micrographs to aid identification, as well as references and resources for further information. This guide will be valuable to fisheries and public health officials as well as all those involved in environmental water quality assessment.

• Language: English
• Publisher: CSIRO PUBLISHING
• Release date: Mar 1, 2024
• ISBN: 9781486318018

Gustaaf M. Hallegraeff

Gustaaf Hallegraeff is an authority on harmful marine microalgae and their impacts on the seafood industry. He is now Emeritus Professor at the Institute for Marine and Antarctic Studies at the University of Tasmania, following positions as Head of the School of Plant Science, and as a principal research scientist at CSIRO. He was awarded the Eureka Prize for Environmental Research and, in 2014, the Yasumoto Lifetime Achievement Award by the International Society for the Study of Harmful Algae. He has also contributed to a number of handbooks on harmful marine microalgae.

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© Gustaaf Hallegraeff 2024

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ISBN: 9781486317998 (pbk)

ISBN: 9781486318001 (epdf)

ISBN: 9781486318018 (epub)

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Hallegraeff GM (2024) Harmful Australian Marine Microalgae. CSIRO Publishing, Melbourne.

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Front cover: (top) Noctiluca scintillans bloom threatening salmon farms off the Tasman Peninsula (Judi Marshall); (bottom, left to right) Derwent plankton with Tripos furca, Tripos muelleri and Dinophysis fortii (Gustaaf Hallegraeff), Karlodinium veneficum (Miguel de Salas), Noctiluca scintillans (Gustaaf Hallegraeff) Back cover: (left to right) Karlodinium veneficum (Miguel de Salas), Gymnodinium catenatum (Gustaaf Hallegraeff), Gambierdiscus lapillus (Gustaaf Hallegraeff)

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The author acknowledges support at the Institute for Marine and Antarctic Studies of the University of Tasmania, where early drafts of this text were first produced.

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Contents

Preface

About the author

Acknowledgements

1. Introduction

Species descriptions

2. Dinoflagellates

3. Diatoms

4. Prymnesiophyta = haptophyta (golden brown flagellates with haptonema)

5. Chrysophyta, class Raphidophyceae (chloromonads)

6. Chrysophyta, class Dictyochophyceae

7. Other flagellates

8. Cyanobacteria (blue–green algae)

Glossary

Further resources

Picture credits

Taxonomic index

Subject index

Preface

Worldwide fish aquaculture production is now approximately equal to that of wild fish capture fisheries¹ and predicted to continue increasing. In Australia the most successful fisheries products are salmonids, tuna, edible oysters, pearl oysters, prawns, lobsters and abalone (combined gross value of about A$3.15 billion and employing 19 000 people), which are all dependent on good water quality. This expansion of production and value will not be without problems and one of the most damaging setbacks – harmful algal blooms – is increasing in global impact. Algal blooms have the potential to wipe out fish farms virtually overnight and contamination of seafoods with algal toxins can poison human consumers of fish and shellfish. During the past three decades, there have been significant increases throughout the world in the economic losses and human health impacts due to harmful algal blooms. Some of this increase in algal blooms may be stimulated by pollution from domestic, industrial and agricultural wastes as well as wastes from aquaculture operations themselves.

This guide arose from 30 years of lecture notes accompanying training courses on harmful marine microalgae targeting Australian shellfish and fish farmers. The first course in 1991 focused on 35 species of potentially harmful algae which at that time had been found in Australian waters, but by 2002 it was necessary to cover some 80 harmful species. The third edition of lecture notes in 2015 included important updates on taxonomic developments (Ceratium, Gambierdiscus, Karenia, Karlodinium, Levanderina, Pseudo-nitzschia, Rhizosolenia, Takayama) as well added a few new problem species (e.g. Azadinium, Pseudochattonella, Stephanocha, Vicicitus, Vulcanodinium), covering some 90 potentially harmful marine microalgae from Australian coastal waters. This 2024 edition updates on taxonomic changes for Anabaena, Alexandrium, Gambierdiscus and Lyngbya but does not add major new problem species, suggesting that this coverage of Australian harmful marine microalgae is close to complete. Most of these species can be readily recognised using a simple monocular microscope. For the purpose of identification, emphasis has been placed on illustrations (line drawings, light micrographs and in some cases electron micrographs). The written species descriptions are accompanied by a summary of the known distribution of the alga in the Australian region, its toxicology and (where available) suggestions for countermeasures. Relevant literature references and a listing of useful websites have been included.

With the help of this guide, fish and shellfish farmers can more effectively monitor for the presence of the algal species described and take the appropriate species-specific counter measures, thereby greatly reducing the hardship caused by algal blooms. This guide will also be valuable to fisheries and public health officials as well as people involved in environmental water quality assessment.

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1. Food and Agricultural Organisation (2022) World Food and Agriculture − Statistical Pocketbook . FAO, Rome. doi: 10.4060/cc2212en

About the author

Gustaaf Hallegraeff received his PhD from the University of Amsterdam in 1976, and worked for 15 years at CSIRO Marine Laboratories in Australia as research scientist/principal research scientist. In 1992 he moved to the University of Tasmania where he became Head of School of Plant Science and Professor, and in 2010 he joined the Institute for Marine and Antarctic Studies, where he currently is Emiritus Professor. In 2004 he was awarded the Eureka Prize for Environmental Research for his research on transport of toxic dinoflagellates via ships’ ballast water, and in 2014 he was honoured with the Yasumoto lifetime achievement award from the International Society for the Study of Harmful Algae. He is a Fellow of the Australian Academy of Technological Sciences and Engineering.

Acknowledgements

I am greatly indebted to my students A/Prof Chris Bolch, Dr Graeme Lush, Prof Martina Doblin, Dr Miguel de Salas, Dr Imojen Pearce, Dr Judi Marshall, Mr Ian Jameson, Dr Juan Dorantes-Aranda, Dr Jorge Mardones, Dr Andreas Seger, Dr Alison Turnbull and colleagues Dr Susan Blackburn, Dr Penny Ajani, Prof Shauna Murray and Dr Steve Brett for working with me on Australian harmful microalgae.

Numerous people provided me with algal bloom samples from Australian waters, especially Ms Jean Cannon (University of Adelaide); the late Ms Barbara McGrath (NSW State Pollution Control Commission); the late Dr Noel Gillespie and Dr Michael Holmes (ex Southern Fisheries Research Centre, Qld); Mr Vas Hosja (Waterways Commission, Perth); the late Dr Jeremy Langdon (Fisheries Department of Western Australia); A/Prof Rick Wetherbee (University of Melbourne); Dr Penny Ajani and Mr Sean Hardiman (ex NSW EPA); and Mr Peter Christy (ex PIRSA SA).

The Institute of Medical and Veterinary Science (IMVS, Adelaide) carried out early mouse bioassays, and Prof Takeshi Yasumoto, Prof Yasukatsu Oshima (Tohoku University, Japan), Dr Andrew Negri (AIMS, Townsville), Prof Dan Baden (University of Miami), Dr Mike Quilliam (NRC Canada), Dr Paul McNabb and Dr Tim Harwood (Cawthron Institute NZ) elucidated the toxin chemistry of Australian samples.

The late Prof Enrique Balech (Argentine) confirmed identification of some of the Alexandrium species, the late Prof Grethe Hasle (University of Oslo) assisted with early identification of Pseudo-nitzschia species, and Dr Jacob Larsen (University of Copenhagen) assisted with identification of the unarmoured gymnodinioid species. I am much indebted to Prof Max Taylor (University British Columbia) and the late Dr Karen Steidinger (Florida Fish and Wildlife Conservation) for initiating me to dinoflagellate taxonomy, and to Prof Øjvind Moestrup (Copenhagen University) for introducing me to nanoflagellate taxonomy.

I acknowledge funding from the Fisheries Research and Development Cooperation (FRDC), Australian Biological Resources Study (ABRS), Australian Research Council (ARC) and early support from the Fishing Training Board of Tasmania.

1. Introduction

What are microalgae?

On land, plants are conspicuous everywhere, whereas in the sea the only plants visible to the casual observer are the seaweeds along our rocky shores and the seagrasses of shallow estuaries. The enormous productivity of the oceans, which cover 70 per cent of the Earth’s surface (our planet should more appropriately have been called ‘Water’!), is based on untold millions of unicellular microscopic algae, collectively called phytoplankton (‘phyto’ = plant; ‘planktos’ = made to wander). These minute plants range in size from 1/1000th of a millimetre to 2 mm and live a floating existence in the upper 200 m of the ocean, where sunlight is available for photosynthesis.

A single litre of seawater may contain as many as 1 million microscopic plant cells. Unlike plant life on land, which is dominated by a single category of organism (the ‘higher plants’), plant life in the oceans includes representatives of as many as 13 algal divisions. More than 10 000 species have been described. These organisms show an immense diversity of form, pigmentation and cellular structure, which are all adaptations to living in the oceanic environment. Phytoplankton species range from the primitive cyanobacteria, which were among the first living organisms on our planet, through the various golden brown algal groups such as diatoms and dinoflagellates, to the green flagellates, which are thought to have been the immediate precursors of the higher plants on the land. A representative selection of phytoplankton species from Australian waters is illustrated in Figs 1, 2 and 3.

These minute plants are critical food for bivalve shellfish (oysters, mussels, scallops, clams) as well as the larvae of commercially important crustaceans and fish. All oxygen-breathing creatures, including humans, are indebted to the phytoplankton because through millenia of photosynthesis they are responsible for every second breath of oxygen we breathe. Furthermore, much of the oil that we use today probably was created millions of years ago when the sun shone on plankton drifting in prehistoric seas and produced, through photosynthesis, minute globules of oil within these cells.

Fig. 1. Representative selection of diatom species from Australian coastal waters; a. Coscinodiscus; b. Thalassiosira; c. Planktoniella; d. Lauderia; e. Skeletonema; f. Leptocylindrus; g. Cerataulina; h. Dactyliosolen; i. Chaetoceros; j. Bacteriastrum; k. Rhizosolenia/Proboscia; l. Ditylum; m. Eucampia; n. Biddulphia/Odontella; o. Asterionellopsis; p. Thalassionema; q. Thalassiothrix; r. Pseudo-nitzschia; s. Nitzschia closterium/Ceratoneis; t. Pleurosigma/Gyrosigma; u. Navicula; v. Surirella; w. Diploneis; x. Cocconeis; y. Licmophora (not to scale).

Fig. 2. Representative selection of dinoflagellate species from Australian coastal waters; a. Prorocentrum; b. Dinophysis; c. Protoperidinium; d. Diplopsalis; e. Scrippsiella; f. Gonyaulax; g. Goniodoma; h. Alexandrium; i. Tripos; j. Gymnodinium; k. Gyrodinium; l. Cochlodinium; m. Amphidinium; n. Polykrikos; o. Noctiluca (not to scale).

Fig. 3. Representative selection of small flagellate species from Australian coastal waters; a–c. Cryptomonads; d–h. Small dinoflagellates, d, e. gymnodinioids (several species); f. Amphidinium; g. Oxytoxum; h. Scrippsiella; i. Euglenoid Eutreptiella; j–l. Green flagellates, j. Pyramimonas; k. Tetraselmis; l. Micromonas/Mantoniella; m–v. Golden brown flagellates, m. Chrysochromulina/Prymnesium; n. Phaeocystis; o–v. Coccolithophorids; o. Emiliania; p. Gephyrocapsa; q. Syracosphaera; r. Calciosolenia; s. Discosphaera; t. Anthosphaera; u. Calciopappus; v. Acanthoica (all flagellates drawn on the same scale: scale bar = 10 µm).

Algal blooms: the good and the bad

The colour of the sea is ever changing. The open sea is blue while nearshore waters are more green, and the water is more transparent in winter than in spring. These differences are caused by the proliferation of microalgae, which just like land plants use dissolved nutrients (nitrate, phosphate), carbon dioxide and sunlight to grow and reproduce. In most cases algal ‘blooms’ are beneficial for aquaculture because they mean more food for shellfish and larval fish. Sometimes the plankton blooms can become so dense (millions of cells per litre) that they obviously discolour the surface of the sea. It is believed that one of the first written references to such a bloom (‘red tide’) appears in the Bible: ‘ ... all the waters that were in the river were turned to blood. And the fish that was in the river died; and the river stank, and the Egyptians could not drink of the water of the river’ (Exodus 7: 20–21).

Algal blooms may also appear yellow, brown, green, blue or milky, depending upon the organism involved. Most water discolourations are caused by motile or strongly buoyant species. Their high concentrations are achieved through a combination of high growth rates and vertical (behavioural) or horizontal (physical) aggregation. Dense algal concentrations are most strongly developed under stratified stable conditions, at high temperatures and following high organic input from land run-off after heavy rains.

The majority of these algal blooms appear to be completely harmless events, but under exceptional conditions, non-toxic-bloom formers may become so densely concentrated that they generate anoxic conditions that cause indiscriminate kills of fish and invertebrates in sheltered bays. Oxygen depletion can result from high respiration by the algae (at night or in dim light during the day) but is more commonly caused by bacterial respiration during decay of