Ecological Studies,Vol. 189 Analysis and Synthesis Edited by M.M.Caldwell,Logan,USA G.Heldmaier,Marburg,Germany R.B.Jackson,Durham,USA O.L.Lange,Würzburg,Germany H.A.Mooney,Stanford,USA E.-D.Schulze,Jena,Germany U.Sommer,Kiel,Germany Ecological Studies Volumes published since 2001 are listed at the end ofthis book. E.Granéli J.T.Turner (Eds.) Ecology of Harmful Algae With 45 Figures,13 in Color,and 15 Tables 1 23 Prof.Dr.Edna Granéli University ofKalmar Department ofMarine Sciences 391 82 Kalmar Sweden Prof.Dr.Jefferson T.Turner University ofMassachusetts Dartmouth Biology Department and School for Marine Science and Technology 285 Old Westport Road North Dartmouth MA 02747 USA Cover illustration:Factors affecting harmful algae (circle in the middle) gains and losses. On the upper half the HA gains include their intrinsic ability to utilize inorganic and organic compounds (mixotrophy), nutrients from anthropogenic origin, and under adverse conditions release allelochemical compounds that kill other algae (allelopathy) or their grazers.On the lower halfthe losses the HA might suffer,in this case no blooms will be formed or damage to the environment will occur. ISSN 0070-8356 ISBN-10 3-540-32209-4 Springer Berlin Heidelberg New York ISBN-13 978-3-540-32209-2 Springer Berlin Heidelberg New York This work is subject to copyright.All rights are reserved,whether the whole or part ofthe material is concerned, specifically the rights oftranslation,reprinting,reuse ofillustrations,recitation,broadcasting,reproduction on microfilm or in any other way,and storage in data banks.Duplication ofthis publication or parts thereofis permit- ted only under the provisions ofthe German Copyright Law ofSeptember 9,1965,in its current version,and per- missions for use must always be obtained from Springer-Verlag.Violations are liable for prosecution under the German Copyright Law. Springer is a part ofSpringer Science+Business Media springer.com © Springer-Verlag Berlin Heidelberg 2006 Printed in The Netherlands The use ofgeneral descriptive names,registered names,trademarks,etc.in this publication does not imply,even in the absence ofa specific statement,that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Editor:Dr.Dieter Czeschlik,Heidelberg,Germany Desk editor:Dr.Andrea Schlitzberger,Heidelberg,Germany Cover design:design & productionGmbH,Heidelberg,Germany Typesetting and production:Friedmut Kröner,Heidelberg,Germany 31/3152 YK – 5 4 3 2 1 0 – Printed on acid free paper Preface In the open sea,primary production is almost totally based on photosynthe- sis by pelagic unicellular or colonial microalgae,collectively known as phyto- plankton.Benthic algae are important primary producers only in extremely shallow water where sunlight sufficient for photosynthesis penetrates to the bottom.Thus,phytoplankton are the basis ofaquatic food chains. Tens to hundreds ofspecies ofphytoplankton belonging to different taxo- nomic units usually coexist in natural assemblages.Phytoplankton are micro- scopic,ranging in size from less than 1µm to more than 100µm,with gener- ation times of no more than a few days. Thus, phytoplankton populations exhibit large temporal variations in response to abiotic factors such as light, temperature,nutrients,and water movement,and biotic factors such as graz- ing, competition, parasitism, and microbial attack. Normally, the standing crop of phytoplankton remains low because these loss factors generally bal- ance rapid intrinsic rates ofgrowth through cell division. Occasionally,increases in one or a few species can overcome losses,such that a given species can dominate phytoplankton assemblages and cause blooms lasting for several weeks or more.Such blooms are due to combina- tions offavorable phytoplankton growth,increased physical concentration by hydrographic or meteorological processes,and reduced losses due to factors such as viruses,sedimentation,and grazing. Some phytoplankton blooms can cause adverse effects.These include oxy- gen depletion,reduced water quality aesthetics,clogging offish gills,or toxic- ity.Blooms ofsuch Harmful Algae (HA) cause Harmful Algal Blooms (HABs). Of the approximately 5,000 known species of phytoplankton,only some 300 species form HABs that are deleterious to aquatic ecosystems in one way or another,and only about 80 ofthese species are known to be toxin producers. Some phytoplankton toxins can be accumulated and/or transported in food chains to higher trophic levels where they contaminate shellfish,making them unsuitable for human consumption,or poison upper-level consumers,includ- ing fish, seabirds, marine mammals, and humans. The economic effects of VI Preface such blooms, including losses to fisheries, tourism, monitoring, and health care can be substantial.In Europe,such losses annually approach 862 million Euros,and in the USA 82 million dollars(see Chap.30). Harmful algae have been the subjects ofscientific and societal interest for centuries.Because blooms oftoxic dinoflagellates were known to occasionally discolor water red or brownish-red,they were,and still are,known as “red tides.”Water discoloration was noted for the lower Nile in the Bible,and Dar- win made microscopic observations ofdiscolored water during the voyage of the HMS Beagle.However,the frequency ofHABs,and the locations affected may be increasing worldwide.In recent years,increases in the numbers ofHA species able to produce toxins have been detected,and new toxins continue to be chemically characterized. It is often assumed that phytoplankton toxins evolved to deter their zoo- plankton grazers. However, most phytoplankton species, including many toxin producers,appear to be routinely grazed by many zooplankters in nat- ural mixed phytoplankton assemblages. Other HA toxins appear to be involved primarily in allelopathy,being released in the dissolved state into sea water and causing deleterious effects on other competitor phytoplankton species.Some HA toxins may be secondary metabolites that are only coinci- dentally toxic.Thus,the role of phytoplankton toxins in the ecology of the algae that produce them remains unclear. HA toxin levels can vary depending on concentrations of nutrients in the water such as nitrogen and phosphorus.In some cases,HA intracellular toxin levels increase in cells grown under unbalanced nutrient conditions.This may be because toxins are the molecules that algal cells use to store or retain sparse nutrients,or because cells under nutrient stress transfer nitrogen from chlorophyll molecules to toxin molecules,causing reductions in rates of cell division but building up toxin levels in the remaining non-dividing cells. Alternatively,some HA species may produce higher amounts oftoxins under nutrient-stressed conditions,thereby more effectively reducing losses to graz- ers and/or by releasing greater amounts ofallelochemical substances to neu- tralize co-occurring phytoplankton species that are competitors for sparse nutrients. Unbalanced nitrogen and phosphorus conditions are often recurrent in coastal waters due to increased anthropogenic discharges ofa given nutrient, relative to others.Thus,it is possible that even ifHABs have not increased in occurrence,the deleterious effects of these blooms may have increased their impacts due to increased toxicity due to unbalanced or anthropogenically altered nutrient ratios. Despite increased research activity, the last major organized published synthesis of HA ecology was the volume originating from the NATO work- shop on harmful algal blooms held in Bermuda in 1996 (Physiological Ecol- ogy ofHarmful Algal Blooms;Springer-Verlag,1998).Although the reviews in Preface VII the volume from the Bermuda meeting were excellent and comprehensive for the time,they are now almost a decade old and somewhat dated by recent developments.Accordingly, we were approached by Springer-Verlag with a request to compile an updated synthesis of HA ecology,organized primarily around processes and questions,rather than organisms.Thus,we invited a global assemblage of active HA researchers to contribute to the chapters in this volume,and many of these same specialists had also contributed to the previous Bermuda meeting volume.All chapters in this volume were peer- reviewed.We hope that this volume will complement other recent reviews and syntheses in Harmful Algaeand other journals,and in international HA meet- ing volumes to identify gaps in our present understanding ofHA ecology and suggest areas for additional research. Kalmar,Sweden Edna Granéli Dartmouth,USA Jefferson T.Turner May,2006 Contents Part A Harmful Algae and Their Global Distribution 1 An Introduction to Harmful Algae . . . . . . . . . . . . . . 3 E.Granéliand J.T.Turner References . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 2 Molecular Taxonomy ofHarmful Algae . . . . . . . . . . . . 9 S.Jansonand P.K.Hayes 2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 2.2 Dinophyta (Dinoflagellates) . . . . . . . . . . . . . . . . . . 10 2.2.1 General Morphology . . . . . . . . . . . . . . . . . . . . . . 10 2.2.2 Dinophysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 2.2.3 Alexandrium . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 2.2.4 Protoperidinium,Prorocentrum . . . . . . . . . . . . . . . . 12 2.2.5 Karenia,Karlodinium,Takayama . . . . . . . . . . . . . . . 13 2.2.6 Amphidinium,Cochlodinium,Gyrodinium . . . . . . . . . . 14 2.3 Cyanobacteria (Blue-Green Algae) . . . . . . . . . . . . . . . 14 2.3.1 Anabaena,Aphanizomenon,Nodularia . . . . . . . . . . . . 14 2.3.2 Microcystis . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 2.3.3 Trichodesmium . . . . . . . . . . . . . . . . . . . . . . . . . 16 2.4 Bacillariophyta (Diatoms) . . . . . . . . . . . . . . . . . . . 17 2.4.1 Amphora,Pseudo-nitzschia,Nitzschia . . . . . . . . . . . . . 17 2.5 Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . 17 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 X Contents 3 The Biogeography ofHarmful Algae . . . . . . . . . . . . . 23 N.Lundholmand Ø.Moestrup 3.1 Biogeography and Species Concepts . . . . . . . . . . . . . . 23 3.1.1 Genetic Variation . . . . . . . . . . . . . . . . . . . . . . . . 24 3.2 Biogeographical Distribution . . . . . . . . . . . . . . . . . 25 3.3 Distribution ofHarmful Species . . . . . . . . . . . . . . . . 26 3.3.1 Dinoflagellates . . . . . . . . . . . . . . . . . . . . . . . . . . 26 3.3.2 Diatoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27 3.3.3 Haptophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . 29 3.3.4 Raphidophyceans . . . . . . . . . . . . . . . . . . . . . . . . 29 3.3.5 Cyanobacteria . . . . . . . . . . . . . . . . . . . . . . . . . . 31 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32 4 Importance ofLife Cycles in the Ecology ofHarmful Microalgae . . . . . . . . . . . . . . . . . . . . . 37 K.A.Steidingerand E.Garcés 4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 4.2 Phases ofPhytoplankton Bloom Development and Life Cycles . . . . . . . . . . . . . . . . . . . . . . . . . . 39 4.2.1 Initiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 4.2.2 Growth and Maintenance . . . . . . . . . . . . . . . . . . . . 41 4.2.3 Dispersal/Dissipation/Termination . . . . . . . . . . . . . . 44 4.3 Environmental Factors versus Biological Factors Affecting Transition . . . . . . . . . . . . . . . . . . . . . . . 44 4.4 Status ofKnowledge and Direction Needed . . . . . . . . . 45 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47 Part B The Ecology ofMajor Harmful Algae Groups 5 The Ecology ofHarmful Dinoflagellates . . . . . . . . . . . 53 J.M.Burkholder,R.V.Azanza,and Y.Sako 5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 5.2 General Ecology . . . . . . . . . . . . . . . . . . . . . . . . . 54 5.2.1 Motility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54 5.2.2 Temperature,Light,Salinity and Turbulence . . . . . . . . . 55 5.2.3 Nutrition:the Continuum from Auxotrophy to Parasitism . 56