Ecology of Harmful Algae

417 Pages·2006·2.97 MB·English

by  E. Granéli

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
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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
Contents XI
5.3 Blooms,Including Toxic Outbreaks . . . . . . . . . . . . . . 59
5.4 Human Influences . . . . . . . . . . . . . . . . . . . . . . . . 60
5.5 Conceptual Frameworks to Advance Understanding . . . . . 61
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
6 The Ecology ofHarmful Flagellates
Within Prymnesiophyceae and Raphidophyceae . . . . . . 67
B.Edvardsenand I.Imai
6.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
6.2 Class Prymnesiophyceae (Division Haptophyta) . . . . . . . 67
6.2.1 Taxonomy,Morphology and Life History . . . . . . . . . . . 67
6.2.2 Distribution and Abundance . . . . . . . . . . . . . . . . . . 68
6.2.3 Autecology and Ecophysiology . . . . . . . . . . . . . . . . . 69
6.2.4 Toxicity and Toxins . . . . . . . . . . . . . . . . . . . . . . . 70
6.2.5 Ecological Strategies . . . . . . . . . . . . . . . . . . . . . . 71
6.3 Class Raphidophyceae (Division Heterokontophyta) . . . . 72
6.3.1 Taxonomy,Morphology and Life History . . . . . . . . . . . 72
6.3.2 Distribution and Abundance . . . . . . . . . . . . . . . . . . 73
6.3.3 Autecology and Ecophysiology . . . . . . . . . . . . . . . . . 74
6.3.4 Toxicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
6.3.5 Ecological Strategies . . . . . . . . . . . . . . . . . . . . . . 75
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
7 The Ecology ofHarmful Diatoms . . . . . . . . . . . . . . . 81
S.S.Batesand V.L.Trainer
7.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
7.2 Toxin-Producing Diatoms,Genus Pseudo-nitzschia . . . . . 82
7.3 Domoic Acid in the Marine Food Web . . . . . . . . . . . . . 83
7.4 Physiological Ecology ofPseudo-nitzschiaspp. . . . . . . . . 84
7.5 Molecular Tools for Studying Pseudo-nitzschia . . . . . . . . 86
7.6 Conclusions and Directions for Future Research . . . . . . . 87
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
8 Ecology ofHarmful Cyanobacteria . . . . . . . . . . . . . . 95
H.W.Paerland R.S.Fulton iii
8.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
8.2 Environmental Factors Controlling CyanoHABs . . . . . . . 97