GE HAB
Global Ecology and Oceanography of
Harmful Algal Blooms
HABs in Eutrophic Systems
This report may be cited as: GEOH AB, 2006. Global Ecology and Oceanography o f Harmful Algal Blooms, Harmful Algal Blooms in
Eutrophic Systems. P. Glibert (ed.). IOC and SCOR, Paris and Baltimore, 74 pp.
This document is GEOHAB Report # 4 . Copies may be obtained from:
Edward R. Urban, Jr.
Henrik Enevoldsen
Executive Director, SCOR
Project Co-ordinator
D epartm ent of Earth and Planetary Sciences
IOC Science and Communication Centre on Harm ful Algae
The Johns Hopkins University
University of Copenhagen
Baltim ore, M D 21218 USA
0 ster Farimagsgade 2D
Tel: +1-410-516-4070
DK-1353 Copenhagen K, Denm ark
Fax: +1-410-516-4019
T el:+45 33 13 44 46
E-mail: scor@jhu.edu
Fax: +45 33 13 44 47
E-mail: h.enevoldsen@unesco.org
This report is also available on the web at:
http://www.geohab.info
http://www.jhu.edu/scor
Primary support for this report and the workshop on which it was
based was provided by the US National Oceanic and Atmospheric
Administration, National Ocean Service, National Center for
Coastal Ocean Science, Center for Sponsored Ocean Research.
http://ioc.unesco.org/hab
Cover photos
Dinophysis acuminata cell. Photo: www.dnr.state.md.us
Karenia m ikim otoi bloom, East China Sea, summer 2005. Photo: J. Li.
Green algae bloom. Photo: www.dnr.state.md.us
Ceratium furca cell. Photo: www.dnr.state.md.us
Gymnodinium cell. Photo: www.dnr.state.md.us
Mahoghany tide in Chesapeake Bay, USA. Photo: P. Glibert
Title page photo
Karenia and Gymnodinium bloom, Leigh Harbour, New Zealand, Oct 2002. Photo: Miriam Godfrey, New Zealand National Centre for
Aquatic Biodiversity & Biosecurity
Back cover photos
Alexandrium taylori bloom, Catalan coast of Spain. Photo: M. Estrada
Clockwise, starting upper left: Dinophysis acuta, Prorocentrum minimum, Pseudo-nitzschia, colony of Microcystis. Photos: www.dnr.
state.md.us
Red tide in Kuwait Bay, Kuwait. Photo: P. Glibert
Copyright© 2006 IOC and SCOR.
Published by IOC and SCOR, Paris and Baltimore, 2006.
GEOHAB
G lobal E cology & O c ea n o g r a ph y
of
H a r m fu l A lgal B loom s
HABs in Eutrophic Systems
(SCOR)
(IOC) UNESCO
S p o n s o r e d b y t h e S c ie n t if ic C o m m i t t e e o n O c e a n ic R e s e a r c h
a n d the
I n t e r g o v e r n m e n t a l O c e a n o g r a p h ic C o m m i s s i o n
of
Edited by: Patricia M. Glibert
W ritten by: J. Icarus Allen, Donald Anderson, Michele Burford, Sonya Dyhrman, Kevin Flynn, Patricia M. Glibert,
Edna Granéli, Cynthia Heil, Kevin Sellner, Theodore Smayda, and Mingziang Zhou
Based on contributions by participants o f the 2005 GEOHAB Open Science M eeting on HABs and Eutrophication, and the
GEOHAB Scientific Steering Committee
Design and layout by: Jane Hawkey
M ay
2006
Table of Contents
Executive Summary
Chapter 1. Introduction
Chapter 2. Development o f the GEOHAB Programme and Its Study o f HABs
in Eutrophic Systems..............................................................................................
Chapter 3. General Understanding o f HABs and Eutrophication: A Synopsis................12
Eutrophication and Its Global Effects......................................................................... 13
Sources o f N utrient Inputs............................................................................................16
The Importance o f Nutrient Quality.............................................................................18
Complexity o f Responses o f HABs to Nutrients..........................................................20
Advancing the Study o f HABs and Eutrophication Through New Techniques
22
M odelling HABs and Eutrophication...........................................................................24
Toward a Consensus on Eutrophication and HAB Proliferation...............................28
Chapter 4. Priorities and Challenges for Understanding the Relationship Between HABs
and Eutrophication............................................................................................................... 32
Key Questions................................................................................................................ 34
Specific Challenges for Further Advancem ent...........................................................46
Chapter 5. Moving Forward in the Study o f HABs in Eutrophic Systems........................ 48
Applying the GEOHAB A pproach................................................................................ 48
Co-ordination o f Activities............................................................................................50
Data Management and Data Sharing..........................................................................50
Protocols and Quality C ontrol...................................................................................... 51
Capacity Building...........................................................................................................51
M odelling Activities.......................................................................................................51
Interaction w ith Other International Programmes and Projects..............................51
References........................................................................................
Appendix I. GEOHAB 2005 Open Science M eeting Programme..
Appendix II. GEOHAB 2005 Open Science M eeting Participants
Appendix III. GEOHAB Scientific Steering C om m ittee.................
Figure Credits...................................................................................
Executive Summary
utrient enrichment of both land and water
is a result of increased human population
growth and many associated activities for
food and energy production, and discharge
of associated sewage and waste. The end result of
nutrient loading to inland and coastal waters is often
an increase in algal biomass, frequently dominated
by one or more species or species groups; this process
is eutrophication. An important consequence of
eutrophication is the increased prevalence of harmful
algal blooms (HABs) that develop high biomass, cause
fish kills, intoxicate seafood, result in oxygen depletion,
and alter trophic interactions. Nutrient enrichment
can stimulate HABs not only directly by stimulation
of growth and biomass, but indirectly in subtle, but
H a r m f u l a l g a l b l o o m s w e r e r e s p o n s ib l e f o r l a r g e f is h k il l s in
AQUACULTURE FACILITIES IN THE E A S T C H IN A S E A IN SUM M ER 2 0 0 5 .
P h o t o : J . L i.
nevertheless significant, ways through alterations in
food web and ecosystem dynamics. The interactions
of these alterations on HAB proliferation are only
beginning to be understood.
W orld-w ide, strong relationships have been observed betw een
increases in nutrient loading and proliferations o f specific types
o f H A B s. In some locales, H A B s have increased in response to
alterations in the type o f nutrient, not only major nutrient forms
such as nitrogen and phosphorus, but changes in the chemical form
o f these nutrients. O rganic, not ju st inorganic, nutrient loading
is increasing world-wide and has been correlated w ith many
blooms o f both dinoflagellates and cyanobacteria. A dvancements
in our understanding o f the physiology o f these organisms has
yielded im portant insights as to why these algal classes respond so
favourably to these nutrients.
4
Increased nutrient loading from human
activities is considered to be one of the reasons
that HABs have been expanding in frequency,
duration, and harmful properties world-wide.
A lthough we have good quantitative estim ates o f many sources
and forms o f nutrient loads, the transform ation processes o f these
nutrients and how they are affected by landscape changes, food
web alterations, and clim atic variations are not well understood.
It is imperative to learn how present trends in nutrient loading
relate to algal blooms in general, as well as how they prom ote the
developm ent o f particular species. The key to th is knowledge is
an understanding o f the ecology and oceanography o f H A B s at
regional and global scales.
The Global Ecology and O ceanography o f H arm fu l A lgal Blooms
(G E O H A B ) Program m e is an international netw ork o f scientists
and projects, under the auspices o f the Scientific C om m ittee
on Oceanic Research (SC O R) and the Intergovernm ental
O ceanographic C om m ission (IO C ) o f U N E S C O . It has as its
fundam ental goal an improved understanding o f H A B population
dynamics through the integration o f biological, chem ical, and
physical studies and application o f advanced observational tools
and m odelling. This report focuses on one o f the overarching
questions o f G E O H A B : T o w h at e x ten t d o e s in creased
S h e l l f is h a n d f in f is h m o r t a l i t y d u e t o
This docum ent outlines the justification, th e priorities for study,
and some o f the new approaches th a t may be brought to bear in
studying the relationships betw een H A B s and eutrophication. The
key questions identified here include:
r e s u l t s in l a r g e
P h o t o s l e f t t o r i g h t : N R C o f C a n a d a , a n d P. G l ib e r t .
•
A re there clusters or specific types o f H A B species th a t are
indicative o f global nutrient increases?
•
To w hat extent do residence tim e and other physical processes
im pact the relationship betw een nutrient loading and H A B
proliferation?
•
H o w do feedbacks and interactions betw een nutrients and
th e planktonic, microbial food webs im pact H A B s and their
detrim ental effects?
•
D o anthropogenic alterations o f the food web, including
overfishing and aquaculture activities, synergistically interact
w ith nutrients to favour H A B s?
•
H o w do anthropogenic changes in land use, agricultural
use o f fertiliser, N O x emissions from vehicles, and global
changes in land cover affect the delivery o f nutrients to coastal
waters and th e resulting incidence o f H A B s? H o w do the
stoichiom etry and quality o f these nutrient sources regulate
th e biological responses favouring H A B s?
•
D o climate change and climate variability have im pacts on
ecosystems th a t augm ent th e im pacts o f eutrophication in the
form ation o f H A B s?
e u tr o p h ic a tio n in flu e n c e th e occu rren ce o f H A B s and th eir
h a r m fu l effects?
This docum ent also serves as an initial road map for the
developm ent o f a Core Research Project w ith in the G E O H A B
fram ew ork on H A B s in E u trop h ic System s. The overall strategy
o f G E O H A B is to apply the comparative approach, to undertake
research th a t is interdisciplinary and international in scope to
encompass the global issues o f H A B events, and to benefit from
the skill and experience o f investigators world-wide. The research
questions and priorities identified herein were developed through
com m unity interaction at an O pen Science M eeting held in
B altim ore M aryland, U SA , in M arch 2005.
HABs
ECONOM IC LOSSES AS W ELL AS LOSS OF PRODUCT FOR CO N S U M PTIO N .
Research on these major priority areas in eutrophication
and its associated effects on HABs is welcome within
the GEO HA B framework. The understanding of
this important issue, and ultimately the management
of nutrient loads and improved prediction and
management of HABs, will require attention from the
global community of scientists.
5
1. Introduction
T
■
EOHAB, the Global Ecology and
Oceanography of Harmful Algal Blooms
Programme, sponsored by the Scientific
M
Committee on Oceanic Research (SCOR)
and the Intergovernmental Oceanographic
Commission (IOC) of UNESCO, is an international
programme to foster and promote co-operative
research directed toward improving the prediction of
harmful algal bloom (HAB) events. GEO HA B has
recognized the impacts of HABs throughout all waters
of the world, but has emphasized events in marine
and brackish waters because of the global significance
N
o c t il u c a b l o o m . H o o d C a n a l , W a s h i n g t o n , U S A , s u m m e r 2 0 0 5 .
P h o t o : W . P a ls s o n , W D F W .
G E dH A B
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B ro c h u re f o r G E O H A B O pen
S c ie n c e M e e tin g o n H A B s a n d
E u tr o p h ic a tio n , 7 -1 0 M a r c h
2005.
6
of these problems and the need for collaborative,
international studies to address them.
H A B s have been associated w ith fish and shellfish kills, hum an
health im pacts, and ecosystem damage thro u g h o u t the world.
C oncurrent w ith escalating influences o f hum an activities on
coastal ecosystems, the environm ental and economic im pacts of
H A B s and consequent challenges for coastal zone m anagem ent
have increased in recent years. The relationship betw een H A B s
and the increasing nutrient enrichm ent o f m any o f the w orld’s
coastal and estuarine environm ents is o f particular concern.
Increasing nutrient loading to coastal and enclosed or estuarine
environm ents is a result o f agricultural, aquacultural, anim al
operations, and industrial and sewage effluents. The relationship
betw een nutrient (both inorganic and organic) loading and
alteration in nutrient supply ratios and many H A B s is now
recognized, but much rem ains to be understood.
GEOHAB is an international programme
directed toward improving the prediction of
harmful algal bloom events.
This report is based on th e G EO H A B Open Science M eeting on
H A B s and Eutrophication and held from 7-10 M arch 2005 in
B altim ore, M aryland, U SA. The program m e and participants
lists are found in A ppendices I and II. This m eeting, th e th ird in
a series o f O pen Science M eetings, brought together international
experts to review the state o f knowledge w ith respect to our
understanding o f the role o f eutrophication in th e proliferation
o f H A B s world-wide and take th e initial steps tow ard designing
research on comparative systems and species to address this critical
global issue.
H A B s in E u trop h ic S ystem s is designed as one o f the Core
Research Projects in the G E O H A B Science and Im plem entation
Plans (www.geohab.info). The research described herein provides a
guide for this C ore Research Project. It w ill serve as a nucleus for
continued planning and w ill be augm ented as research is funded,
results are obtained, and new questions are form ulated. This
docum ent also serves as an invitation to individuals who could not
participate in the G EO H A B Open Science Meeting on H A B s and
Eutrophication.
H a r m f u l a l g a l b l o o m s o c c u r in a l l c o l o r s , r e f l e c t in g t h e
M ULTITU DE OF SPECIES RESPONSIBLE FOR THESE EVENTS W O R LD -W ID E (LEFT
t o r ig h t :
L a J o l l a , C A U S A ; C a m b r id g e , M D
U S A ; S o u t h A f r ic a )
P h o t o s ( l e f t t o r ig h t ) : P. F r a n k s , P. G l ib e r t , a n d G . P it c h e r .
Hawkey, D arlene W indsor and Ji L i, U niversity o f M aryland
C enter for Environm ental Science; and Kevin Sellner and D an
G ustafson, Chesapeake Research C onsortium , for assistance w ith
m eeting preparation. The G E O H A B SSC and the Conference
O rganising C om m ittees are grateful for the financial support for
th e conference provided by th e N ational Oceanic and A tm ospheric
A dm inistration-N ational O cean Service, the US N ational Science
Foundation-D ivision o f O cean Sciences, University o f M aryland
C enter for Environm ental Science, US N ational Office for M arine
Biotoxins and H arm fu l A lgal Blooms, M aryland D epartm ent
o f N atural Resources, Chesapeake Research C onsortium , YSI
E nvironm ental, and G allaudet University.
The members o f the O rganising C om m ittee for the G EO H AB
Open Science M eeting on H A B s and Eutrophication wish to th a n k the
individuals who participated in this m eeting, as it is those people
w ho contributed so substantially to the ideas presented herein.
Special thanks are also given to John C ullen for his contributions
to G E O H A B during its early stages, and to members o f the
past and present G E O H A B Scientific Steering C om m ittee
(SSC, A ppendix III). The contributors to this report wish to
th a n k all those who contributed illustrations and who carefully
reviewed drafts o f this report, especially R aphael Kudela, D ennis
M cG illicuddy, Bob H o w arth , G reg D oucette, A lan L ew itus, Sue
B anahan, and Rob M agnien. The O rganising C om m ittee also
th an k s E d U rban, E lizabeth Gross and Phyllis Steiner, SC O R ;
Judy K leindinst, W oods H ole O ceanographic Institution; Jane
7
2. Development of the G EO H A B
Programme and Its Study of HABs
in Eutrophic Systems
f
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he Global Ecology and Oceanography
of Harmful Algal Blooms (GEOHAB)
Programme was initiated under the
auspices of the Scientific Committee
on Oceanic Research (SCOR) of the International
Council for Science (ICSU) and the Intergovernmental
Oceanographic Commission (IOC) of UNESCO.
Im p le m e n ta tio n
Science FIjii
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Plan
A)
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B
G E O H A B S c ie n c e P l a n ,
G E O H A B I m p l e m e n t a t io n P l a n ,
p u b lis h e d 2 0 0 1
p u b lis h e d 2 0 0 3 .
The Mission and Scientific Goal of GEOHAB
The mission of GEOHAB is to foster international co­
operative research on HABs in ecosystem types sharing
common features, comparing the key species involved,
and the oceanographic processes that influence their
population dynamics.
The scientific goal of GEOHAB is to improve prediction of
HABs by determining the ecological and oceanographic
mechanisms underlying their population dynamics,
integrating biological, chemical, and physical studies
supported by enhanced observational and modelling
systems.
The first G E O H A B planning m eeting was held in H avreholm ,
D enm ark in 1998, and a Scientific Steering C om m ittee (SSC)
was formed in 1999. In 2001, the G EO H AB Science Plan
(G E O H A B 2001) was published, outlining the mission, goals, and
scientific objectives o f the program m e. In 2003, the G EO H AB
Implementation Plan (G E O H A B 2003) was published, representing
an invitation for the com m unity to collaborate on the objectives of
GEOHA B.
G E O H A B is an international program m e to co-ordinate and
build upon related national, regional, and international efforts in
H A B research. The G E O H A B Program m e assists in bringing
together investigators from different disciplines and countries
to exchange technologies, concepts and findings. This takes the
form o f workshops and m eetings, as in the case o f the Baltim ore
m eeting on H A B s and E utrophication, or more specific team s o f
collaborating scientists. G E O H A B is not a funding program m e
per se, but instead w ill facilitate those activities th a t require
cooperation am ong nations and am ong scientists w orking in
comparative ecosystems.
The central feature o f th e G E O H A B Program m e im plem entation
is Core Research, o f w hich H A B s in E u tro p h ic S ystem s is one
priority area. Core Research is comparative, interdisciplinary,
international and directly addresses the overall goals of
G E O H A B as outlined in th e Science Plan. As stated in the
The overall strategy of GEOHAB is to apply the
comparative approach.
Implementation Plan, Core Research comprises oceanographic field
studies conducted in, and application o f models to, comparable
ecosystems, supported by identification o f relevant organism s, and
m easurem ents o f physical, chem ical, and biological processes th a t
control their population dynamics.
The overall strategy o f G E O H A B is to apply the comparative
approach. The comparative m ethod assembles the separate
realisations needed for scientific inference by recognising naturallyoccurring patterns, and tem poral and spatial variations in existing
conditions and phenom ena (A nderson et al. 2005a, G E O H A B
2005). U nderstanding th e responses o f harm ful algae to the
increasing nutrient load o f comparative ecosystems o f the w orld’s
coastal zones w ill assist in prediction o f future patterns as well.
D evelopm ent o f a C ore Research Project in G E O H A B is
based upon the prem ise th a t a comprehensive understanding
o f the population dynamics o f H A B s requires the integration
o f oceanographic studies w ith the application o f models of
comparable ecosystem types. Such comparisons w ill assist in a:
•
•
•
•
definition o f com m on characteristics, including the
groupings o f harm ful species from similar habitat types and
identification o f functional groups;
determ ination o f the prim ary physiological, genetic or
behavioural processes th a t regulate cellular grow th and
toxicity;
identification o f th e im portant physical and chemical
influences over appropriate tem poral and spatial scales; and
developm ent and validation o f technologies for detailed and
extensive m onitoring; establishm ent o f real-tim e observation
platform s.
H a r m fu l a lg a l b lo o m s affect bo th n earsh o r e a n d offsho re w aters
( l e f t t o r ig h t : S w e d e n ; H o n s h u , J a p a n ; B a l t ic S e a ) . P h o t o s : G .
A neer, Y . F u k u y o , a n d K . K o n o n e n .
B io diversity
A d a p tiv e
and
S t r a te g ie s
Biity yog rap hy
N u trien ts
Observation.
Modelling,
and
Prediction
and
E u tro p h ic a tio n
C o m p a ra tiv e
Ecosystem s
M a n a g e m e n t and M itigation
The GEOHAB Science Plan
The GEOHAB Science P/anoutlines five Programme Elements
that serve as a guide to establish the research priorities.
These elements and their overarching questions include:
Biodiversity and Biogeography. What are the factors
that determine the changing distributions of HAB
species, their genetic variability, and the biodiversity of
associated communities?
Nutrients and Eutrophication. To what extent does
increased eutrophication influence the occurrence of
HABs and their harmful effects?
Adaptive Strategies. What are the unique adaptations
of HAB species and how do they help to explain their
proliferations or harmful effects?
Comparative Ecosystems. To what extent do HAB
species, their population dynamics, and community
interactions respond similarly under comparable
ecosystems?
Observation, Modelling, and Prediction. How can
we improve the detection and prediction of HABs by
developing capabilities in observation and modelling?
9
The GEOHAB Programme
Multidisciplinary and Comparative Studies •
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T h e in t e g r a t io n o f f in d in g s f r o m t h e in d iv id u a l P r o g r a m m e
E l e m e n t s d e s c r ib e d in t h e G E O H A B S c i e n c e P l a n is r e q u i r e d
TO ACHIEVE N O T ONLY A N UNDERSTANDING OF
HAB
ORGANISMS AN D
ASSOCIATED EVENTS, BUT ALSO TO DEVELOP PREDICTIVE CAPABILITIES.
S ource:
GEOHAB 2001.
Core research on H A B s in E u trop h ic S ystem s directly addresses
Program m e E lem ent 2, N utrients and E utrophication, o f the
Science Plan. As outlined therein, th e overall objective o f the
N utrients and E utrophication Program m e E lem ent is to determ ine
the significance o f eutrophication and nutrient transform ation
pathways to H A B population dynamics.
The identified specific objectives o f the N utrients and
E utrophication Program m e E lem ent o f G E O H A B include:
•
determ ine the com position and relative im portance to H A B s
o f different nutrient inputs associated w ith hum an activities
and natural processes;
•
determ ine the physiological responses o f H A B and non-H A B
species to specific nutrient inputs;
•
determ ine the effects o f varying nutrient inputs on the
harm ful properties o f H A B s; and
determ ine the role o f nutrient cycling processes in H A B
development.
10
Smaller in scope, but nonetheless equally im portant to the success
o f G E O H A B , are Targeted Research Studies. Targeted Research
Studies address individual objectives outlined in the Science
Plan (G E O H A B 2001). D evelopm ent o f specific models, or
comparative laboratory investigations o f particular H A B species or
species groups, may be investigations th a t fall under th e realm o f
Targeted Research Studies.
This docum ent outlines the justification, the priorities for study,
and the approaches to be taken, in studying the relationship
betw een H A B s and eutrophication. Research on H A B s in
E u trop h ic S ystem s w ill require th e m ulti-dim ensional approaches
o f a Core Research Project, com bined w ith focused or targeted
research, w hich may address specific needs related to individual
species, systems, or m odel development. In the following sections,
a general synopsis o f the current state o f understanding w ith
respect to th e role o f eutrophication in H A B s is provided, followed
by an identification o f the major research priorities, and finally a
roadm ap for addressing these research needs. Research on these
major priority areas in eutrophication and its associated effects on
H A B s is welcome w ith in the G E O H A B fram ew ork (G E O H A B
2003).
3. General Understanding of HABs
and Eutrophication: A Synopsis
f
IM
ƒ
I g
y
Jm
uch has been written in recent years
È
concerning the relationship between
m
HABs and eutrophication (e.g.,
Smayda 1990, Hallegraeff 1993,
Riegman 1995, Richardson and j 0 rgensen 1996,
Anderson et al. 2002, Glibert et al. 2005), but much
uncertainty remains with respect to the process of
eutrophication and how it impacts the propensity for
specific blooms. Although it may seem reasonable to
assume a causal relationship between human activities
and an expansion of HAB events, the underlying
mechanisms are not well known. It is imperative to
M a s s iv e b l o o m s o f t h e d i n o f l a g e l l a t e P r o r o c e n t r u m m i n i m u m
DEVELOP AN N U ALLY IN THE CHESAPEAKE B A Y ,
USA.
PH OTO:
P. G LIB ER T.
learn how present trends in pollution and nutrient
loading relate to algal blooms in general, as well as
N u trien t C h .in g e s
A lg a l R e s p o n s e s
P o le n ile I Im p a c ts
how they may promote the development of particular
species. The key to this knowledge is an understanding
of the ecology and oceanography of HABs at both
regional and global scales. Highlights of current general
EtotlAf m
understanding are provided herein. This is not intended
B arri h e IC itre a I
to be a comprehensive review, but rather a synopsis of
Hum an
where progress has been made and where significant
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LINKED AT M A N Y LEVELS. SO URCE:
12
GEOHAB 2001.
questions still remain. By highlighting the critical
issues, the justification for the Core Research Project on
HABs in Eutrophic Systems will become apparent.
"Eutrophication is the process o f increased
organic enrichment o f an ecosystem, generally
through increased nutrient in p u ts"
Nixon 1995
i
11-10
110-30
120
U M 5 0 -1 0 0
□
■
100-300
m soo
B l >500
Eutrophication and Its Global Effects
M o d e l - p r e d i c t e d e x p o r t o f d is s o l v e d i n o r g a n i c n it r o g e n f r o m
WATERSHEDS TO COASTAL SYSTEMS (KG
“E utrophication” has been defined in various ways (e.g., N ixon
1995, R ichardson and Jorgensen 1996). C entral to all definitions
is the concept th a t the enrichm ent o f water by nutrients causes an
accelerated grow th o f algae and higher forms o f p lant life, which
leads to an undesirable disturbance in the balance o f organisms
present in the water and to the quality o f the water concerned. The
result o f eutrophication is often an increase in to tal algal biomass,
frequently dom inated by one or more species or groups. Such
blooms may have deleterious effects including overgrowth and
shading o f seaweeds and sea grasses, oxygen depletion o f th e water
from algal respiration or decay o f algal biomass, suffocation o f fish,
direct toxic effects on fish and shellfish, suffocation o f fish from
stim ulation o f gili mucus production, and m echanical interference
w ith filter feeding by fish and bivalve mollusks. Deleterious
effects on the benthos may also be considerable. O f additional
concern w ith the developm ent o f high-biom ass algal blooms is the
poor transfer o f energy to higher trophic levels, as many bloom
species are not efficiently grazed, resulting in decreased transfer
o f carbon and other nutrients to fish stocks when they replace
desirable algal species. For example, some H A B species secrete
allelopathic substances th a t inh ib it co-occurring species (P ratt
1966, G entien and A rzul 1990), and suppression o f grazing occurs
above a threshold concentration o f the H A B species (Tracey 1988).
Recently, it has also been shown th a t an increase in the production
o f allelochemicals occurs when some H A B species are subjected to
unbalanced nitrogen or phosphorus conditions, w hich in tu rn are
directly caused by eutrophication (G ranéli and Johansson 2003,
Fistarol et al. 2005a).
E utrophication o f both inland and coastal waters is a result o f
hum an population grow th and the production o f food (agriculture,
anim al operations, and aquaculture) and energy, and is considered
one o f the largest pollution problems globally (H ow arth et al.
2002a, 2005). Population grow th and increased food production
result in major changes to the landscape, in tu rn increasing sewage
discharges and runoff from farm ed and populated lands. In
addition to population grow th, eutrophication arises from the large
increases in the use o f chemical fertilisers th a t began in the 1950s
N K M '2 W ATERSHED'1 Y E AR '1.
S o u r c e : S e it z in g e r a n d K r o z e 1 9 9 8 .
and w hich are projected to continue to escalate in the com ing
decades (Smil 2001, G alloway et al. 2004, G lib ert et al. 2006).
B oth nitrogen and phosphorus are o f concern in eutrophication
(N R C 2000, H o w arth and M arino 2006), but nitrogen has
received far more attention because it often lim its prim ary
production in estuaries and coastal waters, and because the global
application o f nitrogen from synthetic fertilisers is far greater
th a n th a t o f phosphorus (W assm an and O lli 2005). F urtherm ore,
for many regions where phosphorus lim itation has developed, it
may be the result o f excess nitrogen loading. Phosphorus loading,
however, is often cited as th e major cause o f H A B s in freshwaters
(Oliver and G a n f2 0 0 0 ) where nitrogen-fixers often dom inate.
N utrients can stim ulate or enhance the im pact o f toxic or harm ful
species in several ways (A nderson et al. 2002). A t the simplest
level, harm ful phytoplankton may increase in abundance due to
nutrient enrichm ent, but rem ain in the same relative fraction o f
th e total phytoplankton biomass. Even though no n -H A B species
are stim ulated proportionately, a m odest increase in the abundance
o f a H A B species can cause it to become noticeable because o f
its toxic or harm ful effects. A more frequent response to nutrient
enrichm ent occurs w hen a species or group o f species begins to
dom inate under the altered nutrient regime. In deeper freshwater,
estuarine, and coastal marine systems, phytoplankton dom inate the
algal flora. In contrast, macroalgae and benthic microalgae often
dom inate many shallow lakes and poorly flushed estuaries, lagoons,
and upper em baym ents, as well as coral reefs and rocky in tertid al/
subtidal habitats (H arlin 1993). In surface waters across the entire
salinity gradient, there are many examples o f overgrowth and highbiomass blooms by phytoplankton, benthic microalgae (especially
epiphytes), and macroalgae. In many cases, th e responding
dom inant species are not toxic and, in fact, are beneficial to coastal
productivity until they exceed the assimilative capacity o f the
system, after w hich hypoxia and other adverse effects occur. W h en
th a t threshold is reached, seemingly harm less species can have
negative impacts.
13
A S ynopsis
A B O V E : L a r g e b l o o m s o f K a r e n i a b r e v i s o c c u r r e d in F l o r i d a , U S A d u r i n g 2 0 0 5 , r e s u l t i n g in l a r g e f i s h k i l l s . P h o t o s : C . H e i l .
BELOW: L a r g e
P h o t o s : J. Li.
b l o o m s o f K a r e n i a m i k i m o t o i o c c u r r e d in E a s t C h i n a S e a in s u m m e r 2 0 0 5 , r e s u l t i n g in k i l l s o f b o t h w i l d a n d f a r m e d f i s h .
Increases in high-biom ass phytoplankton blooms have been
reported from th e South C hina Sea (Q i et al. 1993), the Black
Sea (B odeanu and R uta 1998), H o n g Kong (L am and H o 1989),
and many other locations, typically in parallel w ith the nutrient
enrichm ent o f coastal waters. In Chesapeake Bay, U SA , high
phytoplankton biomass is typically observed in the spring,
associated w ith high riverine nutrient inputs (G libert et al. 1995,
M alone et al. 1996). These large spring blooms eventually settle
to the bottom , where heterotrophic bacteria process a major
fraction o f the organic m aterial. This can result in depletion o f
oxygen as tem peratures w arm (M alone et al. 1986, Shiah and
D ucklow 1994), leading to hypoxia and m ortalities o f benthic
organisms (e.g., Boynton et al. 1982, M alone et al. 1983, Fisher
et al. 1988, 1992, G libert et al. 1995). As another example, spring
eutrophication from the nitrogen loading o f the M ississippi and
A tchafalaya rivers to the G u lf o f M exico has resulted in enhanced
phytoplankton production and the developm ent o f hypoxia in the
14
G u lf o f M exico, a so-called “dead zone” th a t has altered benthic
food web dynamics and fish habitat substantially (Turner and
Rabalais 1994, C raig and Crowder 2005).
A lthough eutrophication is occurring globally, nutrient export is
not evenly distributed (Seitzinger et al. 2002a, 2005a, H ow arth
et al. 2005, G libert et al. 2006). Inorganic nitrogen export to
coastal waters is estim ated to be highest from E uropean and A sian
lands, although significant discharge also occurs from th e U nited
States and other parts o f the world (Seitzinger and Kroeze 1998).
F urtherm ore, th e rate o f nutrient export to coastal waters has
increased dram atically in recent years in some parts o f the world.
For example, C hina, w hich used less th a n 5 m illion metric tonnes
o f nitrogen fertiliser annually in the 1970s, now uses more th an 20
m illion metric tonnes per year, representing 25% o f global nitrogen
fertiliser consum ption (G libert et al. 2005), leading to significantly
increased nitrogen pollution o f its coastal waters.
A S y n o p sis
others
W h e r e p e o p l e l iv e o n t h e P l a n e t E a r t h , 2 0 0 3 . S o u r c e : N a t i o n a l
N. America
R e s o u r c e s C o n s e r v a t i o n S e r v ic e , U S D A .
L a tin A m e ric a
C o n t r i b u t i o n b y g l o b a l r e g io n t o t h e c o n s u m p t i o n o f t h e w o r l d ' s
The w orld’s hum an population is expected to continue to increase
by 1-2% per year (C ohen 2003), and eutrophication and its
effects, including H A B s, hypoxia, fish kills, and loss o f habitat
are expected to increase in many parts o f th e world. M o st o f these
increases are expected to occur in areas th a t are already affected by
H A B s.
A N N U A L CURRENT USE OF 8 5 M ILLIO N TONNES OF NITROGEN. D A T A FROM
the
I n t e r n a t i o n a l F e r t il iz e r I n d u s t r y . S o u r c e : G l ib e r t e t a l . 2 0 0 5 .
Projections of percent change in nitrogen fertiliser use for the
three decades from 1990 to 2020 for some countries. Plotted
from data provided in Cofala et al. 2001.
15
A S y n o p s is
F r o m ( a b o v e ) s e w a g e d is c h a r g e ( p h o t o : A . K a n a ) , t o im p a c t s o f
Sources of Nutrient Inputs
ATMOSPHERIC EMISSIONS, TO INTENSIVE AQUACULTURE DEVELOPMENT
( p h o t o : P. G l ib e r t ) a n d a n i m a l p r o d u c t i o n f a c il it ie s , t o ( b e l o w )
RUNOFF FROM APPLIED FERTILISER A N D M ANURES (PH O TO : W W W .
k u h n k n ig h t .c o m
) , t h e a n t h r o p o g e n ic s o u r c e s o f n u t r ie n t s a r e
M AN Y .
Global Use of Fertilisers
The change in global consumption of nitrogen and
phosphorus synthetic fertilisers over the past several decades
(from International Fertilizer Industry 2005). Projections
through 2010 are based on an annual increase of 3% (Glibert
and Burkholder 2006).
16
A broad range o f anthropogenic activities result in significant
alteration o f nutrient cycling o f coastal environm ents. Fertiliser
application on land rem ains a major contributor to nonpoint
nutrient pollution, and this source is still increasing at an
alarm ing rate in many geographic regions (Vitousek et al. 1997).
G roundw ater has also been identified as an im portant source o f
nutrients to receiving surface waters. H u m an population grow th
and agricultural practices have increased nutrient loadings to
groundw ater, and th is has the potential to affect algal grow th in
adjacent rivers, lakes, estuaries, and coastal zones. O n local to
global scales, one o f the m ost rapidly increasing sources o f nutrients
to both fresh waters and the coastal zone is th e atmosphere.
A tm ospheric inputs are im portant not only because o f their
m agnitude, but because th e mix o f atm ospheric nutrients - like
other nutrient sources - can stim ulate some phytoplankton species
disproportionately over others. A tm ospheric deposition o f nitrogen
comes from both fossil fuel com bustion and from volatilization
from agriculture and its m agnitude is likely to be underestim ated
in many cases, since gaseous dry nitrogen deposition is seldom
measured (Galloway e t al. 2004, H o w arth et al. 2002a, 2005)
Blooms in the Yellow Sea o f C hina, w hich have escalated in
frequency over the past several decades, have been related to
atm ospheric deposition in addition to direct nutrient ru n off (Z hang
1994). It is estim ated th a t a typical rain event over the Yellow Sea
may supply sufficient nitrogen, phosphorus, and silicon to account
for 50-100% o f the prim ary production o f a H A B event (Z hang
1994). A quaculture ponds and cage culture systems represent
another source o f nutrients, provided as feed or fertiliser and by
the biological transform ations occurring in these high-biom ass
systems. It has been suggested th a t these enriched systems may
prom ote the grow th o f harm ful species not previously detected in
the source water (A nderson 1989, H allegraeff 1993).
A S y n o p sis
M a n u r e N i t r o g e n L e e c h i n g V u l ne r a b i l i t y I ndex
S e w a g e p l u m e m a p a s in d i c a t e d b y
a15N
s ig n a t u r e s o f m a c r o a l g a e
DEPLOYED FOR 4 DAYS IN M A R C H , 1 9 9 8 . D IS T IN C T SEWAGE PLUME (HIG H
a 15N
v a l u e s ) w a s e v id e n t a t t h e m o u t h o f t h e
B r is b a n e R iv e r ,
A u s t r a l i a . S o u r c e : D e n n is o n a n d A b a l 1 9 9 9 .
A n i m a l m a n u r e s a r e a c o m m o n l y a p p l ie d f e r t il is e r . T h is m a p
SHOWS THOSE WATERSHEDS M OST SUSCEPTIBLE TO LEACHING OF M ANURE
NITROGEN TO COASTAL A N D ESTUARINE WATERS. M A N U R E S ARE ONE SOURCE
OF NUTRIENTS TH AT HAVE INCREASED SUBSTANTIALLY IN RECENT YEARS.
S o u r c e : U S D e p a r t m e n t o f A g r ic u l t u r e .
Strong positive relationships have been reported betw een
increasing hum an population and the intensity o f H A B outbreaks
(L am and H o 1989, T rainer et al. 2003). For example, in Tolo
H arbour, H ong Kong, hum an population w ithin the w atershed
grew 6-fold betw een 1976 and 1986, during w hich the number
o f red tide events increased 8-fold (Lam and H o 1989). In Puget
Sound o f W ashington State, U SA , where consistent shellfish
m onitoring has been carried out for decades, a strong positive
relationship betw een the frequency o f one algal toxin, paralytic
shellfish toxin (PST ), and the grow th in hum an population has
recently been reported (Trainer et al. 2003).
However, the im pacts o f differing anthropogenic activities are not
necessarily the same. For example, nutrient delivery associated w ith
sewage may bear little sim ilarity in quantity or com position to th at
associated w ith inputs from agriculture, aquaculture, or dredging
operations. In tu rn , nutrients from these sources may also differ
in quantity and com position from those associated w ith natural
delivery m echanism s such as groundw ater flow and atmospheric
deposition, recognising th a t these sources may also be affected by
hum an activities. The challenge th a t rem ains is understanding the
conditions under w hich specific nutrient forms, or specific nutrient
sources, may im part an advantage to certain H A B species and thus
lead to th eir proliferation.
M oreover, im pacts o f upwelling, storms, m onsoons, and/or
tsunam is may also be sources o f nutrient delivery th a t have to
be distinguished from those above. Therefore, it is o f critical
im portance to distinguish the im pacts o f various activities on
H A B developm ent, and how these im pacts may differ from natural
m echanism s based on w hich nutrients are delivered to the coastal
zone.
Increasing HAB Occurrences
Increasing HAB occurrences in the Tolo Harbour, Hong
Kong, concomitant w ith the increase in human population
in the region. Redrawn by Granéli from Lam and Ho 1989.
S
The relationship between population growth (in millions)
and the average decadal maximum paralytic shellfish toxin
in Puget Sound, Washington State, USA. Replotted from
Trainer et al. 2003.
Average D ecadal Maxim um P ST
1
2
Population (Millions)
17
A S ynopsis
H i g h - b io m a s s b l o o m in T o l o H a r b o u r , H o n g K o n g , r e s u l t in g
The Importance of Nutrient Quality
IN DISCOLORED W ATER, H Y PO XIA, A N D TOXICITY OF FISH A N D SHELLFISH.
P h o t o : M . D ic k m a n .
Foams of Phaeocystis may be caused by the exudation
of protein-rich foams by the algae. Photo by V. Rousseau,
courtesy of the EUROFIAB Science Initiative, 1999.
The change in N:P ratio is related to Phaeocystis blooms in
Dutch coastal waters. From Anderson et al. 2002, based on
Riegman 1995.
I!
18
■ -I- F
M any factors afFect phytoplankton species com position and bloom
developm ent, and am ong these is th e com position o f the nutrient
pool - the forms o f th e nutrients supplied, as well as the relative
abundance o f the major nutrient elements. Efforts to understand
the relationships betw een nutrient loading and algal blooms have
largely focused on to tal nutrient loads and altered nutrient ratios
th a t result from selected nutrient addition or removal. A lterations
in the com position o f nutrient loads have been correlated w ith
shifts from diatom -dom inated to flagellate-dom inated algal
assemblages (Smayda 1990). For example, the num ber o f red tide
events in C hinese coastal waters increased sharply from 1970
to 1993, due in large p a rt to altered nitrogen-to-phosphorus
ratios from increasing use o f synthetic fertilisers and increasing
atm ospheric emissions and deposition o f pollutants.
Perhaps the clearest dem onstration o f the effect o f altered nutrient
supply ratios involves the stim ulation o f non-diatom species
following increases in the availability o f nitrogen or phosphorus
relative to silicate. A prom inent example o f the im portance of
nutrient supply ratios in determ ining phytoplankton species
com position is seen w ith the foam -producing prym nesiophyte
Phaeocystis pouchetii. A 23-year tim e series off the G erm an
coast o f the Baltic Sea docum ents the general enrichm ent of
these coastal waters w ith nitrogen and phosphate, and a 4-fold
increase in the N :Si and P:Si ratios (Radach et al. 1990). This
was accom panied by a decrease in the diatom com m unity and an
increase in the occurrence o f Phaeocystis blooms. A sim ilar tim e
series o f alterations in the N:Si ratio has also been docum ented
for N arragansett Bay, U SA , in w hich a decreased ratio o f diatoms
to flagellates, and increased abundance o f H A B species such as
Heterosigma akashiwo, corresponded w ith an increase in the N:Si
ratio due to excess nitrogen loading from the early to late 1980s
(Smayda and B orkm an, in press).
A S y n o p sis
M any freshwater systems, and freshwater end members o f estuarine
systems as well, have seen a shift in phytoplankton species
com position tow ards bloom -form ing cyanobacteria, including toxic
species such as Microcystis aeruginosa, as phosphorus loads have
increased in these systems (Oliver and G a n f 2000). In tributaries of
C hesapeake Bay, U SA , blooms o f M . aeruginosa in 2003 and 2004
were up to 4 tim es higher th a n a decade earlier (P. T ango, unpub.
data).
A lthough phytoplankton have long been know n to use organic
nutrients in addition to inorganic nutrients (Flynn and B utler 1986,
A n tia et al. 1991), increasingly it has become recognised th a t they
do so under natural conditions. Some species use organic nutrients
for th eir sole nutritional requirem ents, others to supplement their
use o f inorganic nutrients, while still others may use organic
com pounds for their carbon dem ands as well (e.g., G ranéli et al.
1997, 1999, Stoecker 1999). A n increased understanding o f the
bioavailability o f anthropogenically derived organic compounds
has also developed in recent years. The chemical com position of
dissolved organic m atter exported from agricultural watersheds is
not know n, but up to 50% o f this m aterial can be taken up directly
or indirectly by estuarine plankton com m unities (Seitzinger et al.
2002b). The chemical com position, bioavailability, and effects o f
dissolved organic m atter on coastal plankton com m unities vary
depending on its source, the plankton com m unity composition,
and th e season (B ronk2002). O rganic nutrients have been shown
to be im portant in the developm ent o f blooms o f various H A B
species, in particular cyanobacteria and dinoflagellates (e.g., Paerl
1988, G libert et al. 2001) and th e im portance o f this phenom enon
is beginning to be docum ented around the world (e.g., G ranéli
et al. 1985,1999, Berm an 1997, 2001, Berg et al. 2003). A
recent study found th a t in Florida Bay and on the southwest
Florida continental shelf, the cyanobacterial fraction o f the algal
com m unity was positively correlated w ith the fraction o f nitrogen
taken up as urea, and negatively correlated w ith the fraction o f
nitrogen taken up from the inorganic source, nitrate (G libert et
al. 2004). O th er studies have shown th a t some cyanobacteria
M
ic r o c y s t is b l o o m
o n th e lo w e r
St.
J o h n s R iv e r , F lo r i d a ,
2005.
P h o t o : B . Y a te s , w w w . c y p ix . n e t .
The relationship between the percent contribution of urea
to total N uptake by the algal community and the fraction
o fth a t community that was cyanobacteria for Florida
Bay (panel A) and for the southwest Florida continental
shelf (panel B), and the relationships between percent
contribution of NOyto total uptake (panels C and D) for the
same sites. From Glibert and Heil (2005).
C
O
_cro
Q.
o
o
io
m
io
0
40
10 20 00 40 SO 00
b C o n tr ib u tio n o f u re a to N u p ta k e
□.s
0.4
0.3
0.2
0.1
40
80
O*.
100
fto
b C o n tr ib u tio n o f N 0 3" to N u p ta k e
grow faster on urea th a n on other nitrogen sources (Berm an and
Chava 1999, M ulholland et al. 1999). W orld-w ide use o f urea has
increased in recent decades, such th a t urea now represents >50% of
all global nitrogen fertiliser use (G libert et al. 2006).
19
A S ynopsis
“I t may be that as eutrophication progresses through its various stages, changes in life-form
conditions occur which determine which life-form type ofphytoplankter w ill predominated
T ed Smayda (2005) p. 96
Complexity of Responses of HABs to
Nutrients
Prorocentrum minimum blooms in the tributaries of
Chesapeake Bay, USA, have been related to nutrient input.
The extent to which this bloom depends on different forms
of nitrogen is highly dependent on temperature (Fan et al.
2003). Photo: P. Glibert.
Nitrate
A m m o n iu m
T e m p e ra tu
20
The complexity o f the relationship betw een H A B s and
eutrophication is beginning to be appreciated (Smayda 1989,
A nderson et al. 2002, G libert and B urkholder 2006). The
ecosystem response to nutrient enrichm ent, or eutrophication,
is a continual process rather th a n a static condition or a trophic
state (Cloern 2001, Smayda 2005). N utrient availability m ust be
m atched w ith the preferences o f the cells and th eir physiological
conditions, and w ith the physical and trophic structure o f the
w ater colum n at the tim e o f nutrient delivery. A recent conceptual
fram ew ork o f H A B dinoflagellates has been developed. This
is based on distinctive morphological and habitat preferences,
ranging from invasive species th a t dom inate in habitats w ith
enriched nutrient loading to those th a t thrive in more oligotrophic,
stratified systems (Smayda and Reynolds 2001). Large blooms
o f Prorocentrum m inim um , found in many regions affected by
anthropogenic nutrient inputs, are an example o f a species th a t
thrives in habitats w ith enriched nutrient loading (H eil et al.
2005). In contrast, Karenia brevis and K. mikimotoi bloom in open
coastal waters, aggregate in fronts, and are transported by coastal
currents (D ah l and T angen 1993, W alsh et al. 2001).
N utritional mechanism s are complex. In addition to direct
uptake by autotrophs, other pathways o f nutrient acquisition must
be recognized. Indeed, some species, such as the ichthyotoxic
dinoflagellate Pfiesteria piscicida are not autotrophs at all, and
instead, rely virtually exclusively on grazing for th eir nutrition. In
the case o f Pfiesteria, nutrition is provided through a com bination
o f consum ption o f bacteria and other small algae, as well as bits o f
epiderm al tissue o f fish (Burkholder and G lasgow 1997, L ew itus et
al. 1999). Such modes o f nutrition complicate our ability to model
and predict biomass developm ent based solely on nutrient loadings.
Several cyanobacterial species (e.g., Trichodesmium, Anabaena,
Nodularia, Aphanizomenon) are also capable o f fixing nitrogen and
may therefore form massive blooms in circum stances where the
grow th o f other phytoplankton is lim ited by nitrogen.
A S y n o p sis
Thus, while there have been many advances in our understanding
o f nutrient uptake pathways by various species, these pathways and
preferences are complex. It is increasingly recognized th a t certain
species or groups o f species have nutritional requirem ents and
preferences, and therefore may be favoured when the environm ent
is altered in such a way as to increase the relative availability o f the
preferred source.
In addition to species-specific responses and nutrient uptake
requirem ents, the geographic range and biomass o f algae are
affected by physical controls and the behaviour o f the harm ful
algal species. L ong-distance tran sp o rt o f organisms (e.g., Franks
and A nderson 1992), accum ulation o f biomass in response to
water flows, buoyancy regulation, and sw im m ing behaviour
(Kamykowski 1995), and m aintenance o f suitable environm ental
conditions (including tem perature, salinity, stratification,
irradiance, and nutrient supply; W hitledge 1993) are critical to
understanding the ecosystem response to nutrient loads.
O f additional consideration are the trophic interactions controlling
the grow th and accum ulation o f algal biomass. C hanges in food
web structure attributable to over-fishing, habitat degradation,
invasive species, and other factors also interact w ith nutrient
loading to increase susceptibility o f a system to H A B s. W h en
algae are released from predation due to alterations in th e grazing
com m unity, they may proliferate in eutrophic environm ents due
to the abundance o f nutrients (M errell and Stoecker 1998, Stibor
et al. 2004, Vadstein et al. 2004). C hanges in food web structure
affect grazing pressure thro u g h trophic cascading (G ism ervik et al.
1996, P ark and M arshall 2000, T urner et al. 2001); thus, changes
at any level o f the cascade may ultim ately im pact the grazing on the
algae.
O ne area th a t is especially poorly understood is the extent to
w hich, and the mechanism s whereby, nutrient enrichm ent may
lead to the developm ent o f H A B species th a t are toxin producers.
A lthough eutrophication may be associated w ith increasing
numbers o f high-biom ass blooms or other H A B events, the specific
M a n y b l o o m - f o r m i n g f l a g e l l a t e s h a v e p h a g o t r o p h ic c a p a b i l it ie s
- THE AB ILITY TO ENGULF A N D INGEST PARTICULATE M ATERIAL FOR
N U TR ITIO N AL PURPOSES, SUCH AS THIS PFIESTERIA CELL FEEDING O N A
C R YPTO M O NAD CELL. P H O T O : M . PaR R O W .
relationships leading to increased frequency o f toxin producers,
and th e increased production o f toxin w ith in these organisms
are often poorly characterized. A s many toxins are considered
to be secondary metabolites, th eir production w ill depend on
th e physiological condition o f the cells (Flynn and Flynn 1995,
G ranéli et al. 1998, G ranéli and F lynn 2006). Differences in toxin
production may therefore be related to changes in grow th rate or
th e grow th conditions o f an organism. For Pseudo-nitzschia, for
example, more domoic acid is produced under silica or phosphorus
lim itation th a n under nitrogen lim itation, likely due to the fact th at
domoic acid is a nitrogen-rich molecule (Bates et al. 1989, 1991).
Furtherm ore, when adapted to its nitrogen source, Pseudo-nitzschia
appears to produce more domoic acid when grow n on urea th a n on
other nitrogen sources (A rm strong and Kudela 2003). G row th on
urea is also know n to change the toxin content and composition
in the genus Alexandrium (D yhrm an and A nderson 2003). These
studies underscore th e im portance o f nutrient source as well as
physiological condition in toxin production by H A B species.
A nother area th a t is starting to gain attention is how some
H A B species increase production not only o f toxins but also
o f allelochemicals, particularly under conditions o f nitrogen or
phosphorus deficiency. These allelochemicals enable such species to
utilize the “scarse” nutrient resources by inhibiting and/or killing
th eir com petitors (other algae) and even th eir grazers (G ranéli
and Johansson 2003a, T illm an n 2003, Fistarol et al. 2005). In
such situations, the effects o f these allelochemicals are enhanced
even further, as the other algae are debilitated by nutrient
depletion (Fistarol et al. 2005). M onospecific blooms are often
found for such species w ith the capability o f producing potent
allelochemicals, as in th e case o f Prymnesium parvum (G ranéli and
Johansson 2003b, G ranéli and H ansen 2006).
21
A S ynopsis
A s a further, more fundam ental complication, different strains
w ithin the same species often respond to nutrients differently. A
com m on m isunderstanding is th a t the characteristics o f one strain,
m aintained for years under highly artificial laboratory conditions,
are representative o f all strains o f th a t species in the natural
environm ent. This assum ption overlooks the fact th a t for nearly
all algal species studied, different strains w ithin the same species
generally have shown m arked differences in fundam ental traits
such as grow th characteristics, toxicity, bloom -form ing behaviour
and responses to nutrients and other environm ental conditions
(Cem bella et al. 1987, W ood and L eatham 1992, A nderson et
al. 1994, B urkholder et al. 2001, 2005, Burkholder and G libert
2006). In the case o f the cyanobacterium Microcystis aeruginosa,
high levels o f nitrogen and phosphorus were found to favour the
grow th o f toxic strains over non-toxic strains (Vezie et al. 2002).
There is much yet to be understood w ith respect to the response
o f individual species to nutrient loading, and how changes in both
quantity and quality o f nutrient loading, in conjunction w ith the
physical and trophodynam ic state o f the receiving waters, may
lead to H A B s. It is therefore im portant to study the grow th and
behaviour characteristics o f strains o f a particular species from a
num ber o f globally-distributed locations and to do so under natural
nutrient concentrations and to collect data adequate for the support
o f m odelling (Flynn 2005b).
A u t o n o m o u s i n s t r u m e n t a t i o n is p e r m i t t i n g a c q u i s i t i o n o f a r a n g e
OF DATA, IN C LUDING NUTRIENT CONCENTRATIONS, BEFORE , DU RIN G ,
A N D AFTER BLO O M S, AD VA NCING OUR UNDERSTANDING OF THE DYN A M IC
RELATIONSHIPS BETWEEN NUTRIENTS A N D H A B OUTBREAKS. PH O TO S LEFT
t o r ig h t :
W.
B o ic o u r t a n d
M.
T r ic e .
Advancing the Study of HABs and
Eutrophication Through New Techniques
The potential for advances in understanding o f the im pacts o f
nutrient pollution on, and relating eutrophication to, H A B s and
th eir proliferation is large. N ew and b etter tools are providing
m ethodologies for addressing questions related to the complexities
o f the nutrient pool, th e tim e and space scales on w hich nutrients
are delivered, and algal nutrition. O nly a few tools are illustrated
here.
A classic dilem m a in assessing w hether, and, to w hat extent,
nutrients are stim ulatory to a given H A B is th a t the reporting
and sam pling o f bloom events typically occurs after the H A B has
developed. By th a t tim e, many nutrients are consum ed, leading to
the potentially erroneous conclusion th a t nutrients are unavailable
and therefore u nim portant. T raditional approaches for collecting
inform ation on nutrient distributions, such as weekly or bim onthly
sam pling, are also inadequate to detect the short-lived nutrient
pulses th a t often follow meteorological events. D evelopm ent o f
in situ nutrient m onitors has provided a means to begin resolving
the all-im portant antecedent conditions and to provide sufficient
resolution o f the tem poral scale o f bloom events. Use o f these types
o f in situ instrum ents in conjunction w ith other rem ote m ethods
for resolving additional environm ental characteristics (Babin et al.
2005) may yield the resolution necessary to define the ephemeral
changes in nutrients th a t can be significant to phytoplankton cells.
The H A B research field has led the oceanographic com m unity
in species detection. Advances in molecular approaches are also
allowing, for some species, the resolution o f the response o f an
individual population w ithin a mixed species assemblage. For
22
A S y n o p sis
Enzyme labeled fluorescence (ELF)
example, major advances in m arine microbial genomics, such
as the sequencing o f Thalassiosira pseudonunni! (A rm brust et al.
2004, D oney et al. 2004) are providing insight into the genetic
capacity o f selected algal models. In recognition o f its significance,
the Joint G enom ic Institute (http://w w w .jgi.doe.gov) is now
sequencing the Aureococcus anophagefferens genome (~32Mb). The
availability o f this first full H A B genome w ill allow researchers
an unprecedented ability to assess physiological potential in this
species, and to examine the genome for clues as to how th is model
organism uses nutrients and w hat makes it so successful in certain
coastal systems. These genomic advances are driving technology
developm ent, and as the cost o f sequencing becomes affordable,
there are an increasing num ber o f studies th a t are exam ining
transcriptional processes in key organisms (Lidie et al. 2005).
Tools such as quantitative polymerase chain reaction (PC R ) and
m icroarray chip technology are becom ing available, and these
approaches w ill increasingly allow scientists to assay (at the level of
gene transcription) how different H A B species respond to changes
in their exogenous nutrient environm ent. A dditional advances
in protein detection and characterisation w ill help to further
define how H A B species respond to eutrophication. For instance,
we can now track the phosphorus physiology o f Prorocentrum
minim um using antibody probes for a phosphorus-regulated protein
(D yhrm an and Palenik 2001). The H A B science com m unity is
now poised to bring the full potential o f these exciting advances to
the study o f H A B s and eutrophication.
Furtherm ore, flow cytom etry, a m ethodology for rapidly
m easuring intrinsic or applied (stained) optical characteristics of
individual cells, has been used to study the occurrence, abundance,
physiology, and diversity o f aquatic m icroorganism s for the past
tw o decades. This technology has been increasingly applied to
the study o f H A B species, for example, to generally enumerate
and specifically identify harm ful algal cells in cultures (Shumway
and Cucci 1987, Vrieling et al. 1997) and natural samples (Costas
and L opez-R odas 1996, Becker et al. 2002). This tool also has
recently advanced our understanding o f H A B s and th eir relation
to nutrients and for tracking changes in the complex structure
o f aquatic microbial com m unities (including viruses, pathogenic
L E F T : P e r c e n t a g e A n t ib o d y L a b e l e d .
R I G H T : C e l l - s p e c if ic
DETECTION OF ENZYME AC TIV IT Y : E N Z Y M E LABELED FLUORESCENCE ( E L F )
DETECTS A LKALIN E PHOSPHATASE AC TIVITY IN A FIELD SAMPLE FROM THE
O regon C o ast. S ource a n d pho to s: S. D y h r m a n .
bacteria, and harm ful algae) as related to seasonal cycles, nutrients,
or bloom age (e.g., L i and Dickie 2001, Jacquet et al. 2002). Such
studies, including recent in situ flow cytom etric investigations
o f phytoplankton assemblages, are providing valuable insights
about biological factors (e.g., infection, com petition, grazing) th a t
influence the occurrence and distribution o f H A B s. Recently, the
cell-sorting capacity o f some flow cytom etres has been applied,
as well, to assess modes o f nutrition by H A B species (Parrow and
B urkholder 2003).
Knowledge is also advancing about th e chemical composition
o f the nutrient environm ent in w hich H A B s may thrive. The
chemical composition o f th e dissolved organic nitrogen pool has
long been recognised to be complex, consisting o f a m ixture of
multiple com pounds (B ronk 2002). Electrospray ionisation mass
spectrom etry is a tool now allowing greater characterisation than
has been possible in the past. In contrast to past methodologies
for studying the organic m atter pool - w hich were mostly lim ited
to bulk analysis o f total carbon or nitrogen, analyses o f a few
individual com pounds (e.g. urea, am ino acids, specific proteins), or
com pound classes th a t account for a small percent o f total dissolved
organic m atter (e.g., total carbohydrates, total proteins; B ronk
2002) - electrospray ionisation mass spectrom etry allows for the
exam ination o f a large suite o f individual com pounds in natural
mixes o f dissolved organic m atter. This technique also provides
molecular w eight inform ation o f ionisable com pounds (in the form
o f a m ass-to-charge ratio, m /z, w hich equals molecular w eight for
singly charged compounds), and a measure o f concentration as ion
abundance (Seitzinger et al. 2005b). As more researchers use this
type o f instrum ent, com pound libraries w ill be developed, allowing
characterisation o f individual com pounds, and com parison am ong
p atterns in use o f specific com pounds in comparable ecosystems
and by comparable species in different environments.
23
A S ynopsis
“
A subtle, but pervasive, achievement o f biological oceanography is that modelling has
become a mainstream activity; it permeates so much o f our work that graduate students in
the discipline assume it is integral to biological oceanography. Modelling was at one time an
esoteric craft practiced by a gifted few ; now it is the norm. Today’s biological oceanography
graduate student is more likely to have a model than a microscope.”
Richard T. Barber and Anna K. Hilting (2000), p. 19
Modelling HABs and Eutrophication
Fundam ental research on H A B s m ust be guided by and validated
w ith observations o f phytoplankton dynamics in nature. To
determ ine why H A B s occur, it is necessary to describe the
tem poral and spatial developments o f the targ et species in specific
ecosystems. This requires observation and m odelling o f the
physical-chemical-biological interactions th a t support the specific
life strategies o f H A B species in relation to other members o f the
plankton comm unity. Consequently, measurem ents o f physical
and chemical properties and processes, along w ith quantitative
detection and characterisation o f the plankton, m ust be made
w ithin a spatial and tem poral fram ew ork th a t is appropriate for
characterising bloom dynamics. It is also critically im portant to
param etrise the environm ental conditions leading up to a bloom
event, and not ju st those associated w ith the term inal phases o f a
bloom and its subsequent decline.
Effective interaction betw een observationalists and modellers
is essential (Flynn 2005b). It is typical th a t w ith in models, the
more complex th e description is o f the physical environm ent, the
less complex the description is o f the biology. Similarly, the more
complex the biology, the less complex is the model o f the physics.
A n example o f model hierarchy illustrates this.
Z ero-dim ensional models are useful for describing complex
biological interactions, but w ith reduced physics. These models
can provide test-beds to develop and check param etrisations o f
chemical-biological processes such as nutrient uptake, grow th,
grazing or production o f toxins. They are appropriate for detailed
descriptions o f processes w ith in the cell (e.g., interaction o f the
internal nutrient pools and regulation o f toxin production; Flynn
1998). For advanced H A B models, processes such as these can
be incorporated into dynamic models o f nutrient assimilation,
photosynthesis and pigm ent synthesis as they influence grow th
kinetics or toxin production (e.g., John and Flynn 2002, Flynn
2005b). Such form ulations are necessary to lin k nutrient
assim ilation and grow th processes w ith variable nutrient quotas,
24
cell pigm ents, and bio-optical signatures o f phytoplankton
(Schofield et al. 1999).
F u rth er complexity can be provided through one-dim ensional
w ater colum n models th a t allow the inclusion o f additional
processes, such as m ixing, sinking and buoyancy, nutrient uptake,
and benthic-pelagic coupling in a vertically structured environm ent
(light, salinity, tem perature, nutrients). Sim ulations can be related
directly to experim ents in mesocosms and to observations in the
field, if advection is not too im portant. M oreover, water colum n
models can be ru n w ith very high vertical resolution to study
processes in th in layers (D onaghay and O sborn 1997). Extension
to tw o-dim ensional models is useful for exam ining the physicalchemical-biological interactions th a t influence th e distributions
and population dynamics o f phytoplankton, for example, in coastal
fronts (Franks 1997). W ith the recognition th a t lig h t and nutrient
history play a major role in cell grow th and metabolism (e.g.,
Flynn 2002), the use o f L agrangian ensemble approaches (W oods
and B arkm ann 1993, A nderson et al. 2005) may be necessary to
unravel the population dynamics o f H A B s in nature.
T hree-dim ensional, physical-chemical-biological coupled models
are required to simulate the population dynamics o f H A B s
comprehensively in an oceanographic context. G iven the scales o f
biological and physical variability in response to th e local forcing
and far-field effects, three-dim ensional models m ust have the
flexibility to allow different resolutions. O w ing to th eir modular
model structure, three-dim ensional circulation models can be
used for problems w ith different complexity o f the corresponding
biological processes. Examples o f a simplified biological approach
include the study o f driftin g cells th a t spread in response to
w ind-driven circulation or populations th a t accumulate at
fronts. M ore complex models w ith physiological com ponents,
including dynamics o f grow th, chemical com position, and nutrient
assim ilation allow, in principle, comprehensive explorations o f
the physical, chem ical, and biological interactions th a t determ ine
population dynamics. These models can study th e roles o f sinking,
buoyancy, advection, shear flows, and small-scale turbulence. So, in
A S y n o p sis
METABOLISM INFLUENCED DINOFLAGELLATE DIEL VERTICAL MIGRATION
external
NlTR.QSEJti
ÜIVIs a n
<
DËSCËNT A5CENÎ
r r \
h
nui or
Listii
INTEHBfTY
a x is
P M O T Ö S t M TM ATË
IC A R B O H Y D H A T E O R U H D |
addition to accounting for th e physiology o f algal grow th and toxin
production, we need to determ ine th e rules th a t govern behaviour
(e.g., vertical m igration and variable sinking rates) and the links
betw een behaviour and physiology (Cullen and M acIntyre 1998,
Kamykowski et al. 1999).
T h e c o m p l e x i t ie s o f m o d e l l i n g p o p u l a t i o n d y n a m i c s a r e il l u s t r a t e d
HERE FOR A SPECIES TH AT UNDERGOES VERTICAL M IG R A TIO N . T H E
FUNCTIO NS (CIRCLED LETTERS) TH AT M UST BE PARAMETRISED IN THIS M O D EL
INCLUDE EN VIRO NM ENTAL FORCING, PHYSIO LOG ICAL RATE PROCESSES,
BIO C HEM ICAL POOL CONCENTRATIONS, CELL D IV IS IO N , A N D BEHAVIOUR.
S o u r c e : G E O H A B 2 0 0 1 , m o d if ie d f r o m K a m y k o w s k i e t a l . 1 9 9 9 .
Indeed, many models could be argued as having serious flaws in
th eir biological structure (Flynn 2005a, b). W hile experim ental
research tends to highlight differences am ong systems, modelers
tend to try to identify unifying them es. W hile simplicity is the
goal for all m odelling efforts, the extent and means by w hich
this is achieved is controversial. M any physical and biological
oceanographers claim th a t model com ponents are oversimplified.
The m ain problem is th a t while physics is an exact science,
biology is not; we simply know too little about the functioning
o f H A B ecosystems. As a consequence, biological models often
rely on outdated biological knowledge. Some im portant biological
processes are often not considered at all, for example, use o f
dissolved organic m atter (D O M ), allelopathy, mixotrophy, and
prey selectivity related to nutrient status.
Effective interactions betw een observationalists and modellers
w ill depend on easy interactive access for the non-specialist to
m odelling tools, including the com ponent models. In tu rn , the
interaction o f observations and m odelling also requires effective
means for visualisation and developm ent o f interactive capabilities.
Predictions o f H A B -specific coupled models w ill be im proved by
well designed m onitoring and use o f data assim ilation techniques
to integrate real-tim e and near-real tim e data into a ru n n in g model.
D ata assim ilation can thus provide better now -cast predictions of
conditions during process studies. These predictions are useful for
adaptive sam pling, and they address a principal goal o f G E O H A B ,
the early w arning and prediction o f H A B s.
W h ile much progress has been made, there are a num ber o f
critical issues w ith respect to collection o f data th a t impede our
progress to m odel H A B occurrence. These include (1) the range
o f data types, (2) th e frequency o f m easurem ent, and (3) the
units o f m easurem ent. W h ile the im portance o f the first tw o are
widely recognized in experim ental studies, the th ird is not. The
consequence o f failings in any o f these three areas is th a t most
experim ental studies (laboratory and field) are o f little or no use
in the developm ent o f models (Flynn 2005b). In the same way
th a t experim ents should be designed at th e outset to yield data
amenable to statistical analysis, so they should also generate data
suitable for the support o f m odelling efforts. To highlight one
particular problem in th is regard, the routine m easurem ent of
H A B abundance using chlorophyll in vivo fluorescence gives data
o f poor value to modellers, as the chlorophylkcarbon (C hl:C ) ratio
changes w ith nutrient status and irradiance (including self shading
as the bloom develops), and th e ratio betw een the fluorescence
signal and chlorophyll also varies w ith nutrient status (K ruskopf
and Flynn 2006). F urther, the use o f chlorophyll as a biomass
indicator for organisms w ith a high m ixotrophic ability is arguably
illogical. For example, the dynamics o f Pfiesteria piscicida could
not be m odelled as a function o f chlorophyll as it does not contain
chlorophyll, other th a n th a t w hich it has eaten. Indeed, for many
physiological processes, expressing th e relationship as a function of
chlorophyll versus carbon yields vastly different relationships.
The problem o f param etrising H A B biomass is also not resolved
by identification o f individual species. To describe and model
population dynam ics, distributions o f the targ et organisms
m ust be determ ined at the species level; other members o f the
25
A S ynopsis
jr • • • J
'ís
'h y to p la n k to n
DON U p ta k e'
C h em ical L eeching
& Bacterial P ro ce sse s
E xcretion &
^ M o r t a li t y
A SCHEMATIC D IA G R A M OF A NITR OG EN -BASED M O D EL OF M IX ED -LA YER
PLANK TO N A N D NITROGEN CYCLING SH OW ING THE FLOW OF NITROGEN
A M O N G CO M PARTM ENTS. SO URCE: D . KELLER , R . H O O D , A N D THE
I n t e g r a t io n a n d A p p l ic a t io n N e t w o r k , U n iv e r s it y o f M a r y l a n d
C e n t e r f o r E n v i r o n m e n t a l S c ie n c e , w w w . i a n . u m c e s . e d u .
com m unity should be identified and quantified as taxonom ic or
functional groups. This analysis is traditionally done thro u g h visual
microscopic exam ination, a slow and tedious process th a t is poorly
suited for research on the dynamics o f H A B s. Simply, resources
are often inadequate to obtain and analyse enough samples to
describe adequately the distributions o f species in space and tim e.
A lso, some species are extremely difficult (e.g., w ithin the genus
Alexandrium) or impossible (e.g., Pseudo-nitzschia) to distinguish
w ith light microscopy alone. These constraints also ham per efforts
for routine m onitoring. A utom ated m ethods are needed and several
approaches are being pursued, including antibody probes (Shapiro
et al. 1989, A nderson et al. 2005b), nucleotide probes (Scholin
et al. 1999, A nderson et al. 2005b), and other assay m echanism s
such as quantitative P C R (e.g., Coyne et al. 2006) th a t can be
adapted for use in sem i-autom ated bulk-sample analysis or single­
cell analysis using flow cytom etry, depending on the approach.
In the m eantim e, bio-optical oceanographers continue efforts
to extract inform ation on species com position o f phytoplankton
from measurem ents o f ocean colour and other optical properties
o f surface waters (Stuart et al. 1998, C io tti et al. 1999, Schofield
et al. 1999, K irkpatrick et al. 2000). Even where it is possible to
m onitor specific algal groups, however, it m ust be recognised th at
presence alone does not confer the potential for a toxic or noxious
bloom event. To describe and understand ecological controls on the
activities and effects o f H A B s in nature, physiological status and
toxicity o f the algae m ust be determ ined along w ith identification
and quantification. Fortunately, labelling and detection m ethods
sim ilar to those for identifying species can be used to assess
biochem ical or physiological properties such as the presence o f a
toxin (Lawrence and Cem bella 1999), enzyme activity (G onzálezG il et al. 1998), and photo synthetic capability (O lson et al. 1996).
26
Inherently, all models involve some form o f simplification because
it is not feasible to include every organism or every species - and
the interactions am ong them - explicitly. M any models aggregate
the biological com ponents and abstract them into functional
groups or com partm ents. Such functional groups may represent,
for example, the m ain roles o f production (e.g., phytoplankton),
consum ption (e.g., Zooplankton, fish) and decom position (e.g.,
bacteria). Functional group models are com m only used to simulate
phytoplankton and nutrient cycling, but are frequently extended to
include Zooplankton, detritus, and the microbial loop. There is an
optim al balance betw een model detail and perform ance (Fulton et
al. 2003). Too much complexity leads to uncertainty (particularly
in param étré definition) and problems in interpretation o f the
models’ dynamics and predictions; too little complexity and the
models cannot reproduce realistic behaviour. However, a m eta­
analysis o f data for process-oriented planktonic ecosystem models
(based on 153 studies published betw een 1990 and 2002) indicates
th a t increasing complexity does not improve th e fit w ith data
(A rhonditsis and B rett 2004, A nderson 2005). Ultimately, the
selection o f model complexity should be driven by questions being
asked o f th e system under study, but lim itations on the complexity
may arise from the data available. M uch o f the research supporting
our phenom enological understanding o f H A B species physiology is
inadequate for the param etrisation o f models. Research is required
to seek a more rational determ ination o f model complexity to
address the problems under consideration (M oll and Radach 2003).
This m ust also be considered w hen submodels are lifted from one
m odelling system and applied to a new m odelling system - the
original caveats in th e design and use may well be ignored.
In the context o f H A B s, th e developm ent o f planktonic models
w ith a stronger physiological basis are required if we are to obtain
more accurate simulations. The key stages in defining the structure
o f an ecological model are to concentrate the degree o f resolution
or representation to the m ain targ et species and to make increasing
simplifications or decrease the resolution both up and dow n from
the target level (de Young et al. 2004).
A S y n o p sis
The Rhomboidal Modelling Approach
0.1
Predators
H A B /Z ooplankton
focus
at
&
o
0,06
(5
>-■
£
0,04
d ia to m s
Life h isto ry
W ith o u t life
\ h isto ry '
£
Greatest fu n ctio n a l
c o m p le x ity at th e
area o f focus
N u trie n t/B a cte ria /
Protozoan focus
C hem istry
1
10
100
1000
Ir ra d ia n c e ( p m d p h o to n s n r 2 s e c 1)
Functional co m p le xity
G e n e r a l t r e n d in t h e v a r i a t i o n s in t h e c h l o r o p h y l l a : C r a t io f o r
S c h e m a t ic i l l u s t r a t i n g t h e r e l a t io n s h i p b e t w e e n t r o p h ic l e v e l
PROKARYOTES A N D FOR DIATOM S AS A FUNC TIO N OF THE IRRADIANCE AT
A N D FU N C TIO N A L COM PLEXITY. T H E R H O M BO ID ILLUSTRATES THE REGION
W H IC H THEY WERE G RO W N . REVISED A N D REDRAWN FROM M a c I n TYRE A N D
OF PRIMARY FOCUS FOR H A B M O D ELS. REVISED FROM DE Y O U N G ET AL.
C u lle n 2 0 0 5 .
200 4.
To model H A B s, we need to consider representing the target
species explicitly, possibly including th e key stages o f its life
history and its links to the environm ent. For the H A B s th a t are
m ixotrophs, such an approach may be more difficult, as the H A B
may serve as both prim ary producer and consumer. M odelling
m ixotrophy is probably one o f the m ost challenging activities in
plankton modelling.
A n im portant aspect o f m odelling data is th a t it allows an
expert user to infer from it aspects o f the system th a t the model
is not able to simulate directly. In the same way th a t a w eather
forecaster interprets inform ation about pressure and moisture
fields from a num erical w eather prediction model to infer w hat
the w eather w ill be, a marine environm ental forecaster may be
able to take inform ation from a numerical ecosystem prediction
m odel to predict aspects o f the ecosystem not directly simulated.
For example, we know th a t H A B events often coincide w ith
distorted nitrate:phosphate ratios and low turbulence, and th a t
toxin production often occurs when the phytoplankton are nutrient
stressed. C urrently, we cannot make species-specific simulations
o f H A B s but we can simulate these indicators. In principle, we can
combine inform ation from hydrodynam ic and ecosystem models to
provide probability-based risk maps o f H A B occurrence.
Modelling is intricately linked with observation and
experimentation, and both models and predictive systems
will be improved as new analytical approaches aid
experimental research, and new monitoring systems yield
data on time and space scales appropriate for the processes
of interest.
A generic m odelling system may facilitate comparative studies,
by providing a consistent m odelling fram ew ork th a t can be
applied in all regions. This fram ew ork needs to be m odular to
allow simulations o f differing complexity according to the task at
hand. C rucial to this is a consistent model evaluation procedure
on a num ber o f levels (temporal, spatial, and functional) and the
generation o f error statistics. O u r current lack o f physiologically
robust species-specific H A B models implies th a t forecasting o f a
species-specific H A B event is probably not consistently achievable
in the short term . A lthough m odelling has evolved enormously
as a discipline and as an integrated activity th roughout all o f
oceanography and ecology (e.g., Barber and H iltin g 2000), if our
understanding o f events surrounding the developm ent o f H A B s is
to be judged by our ability to simulate th eir occurrence, then there
is much w ork to be done. The developm ent o f a new generation
o f physiologically robust H A B models w ill require better synergy
am ong modellers, observational approaches, and experim entalists.
P ro cess
S tud ies
E a rly W arm n g
and Prediction
S y stem s
27
A S ynopsis
o>
Tbticbatiiiii
Longitude (deg.)
Toward a Consensus on Eutrophication
and HAB Proliferation
In developing the recom m endations and priorities for study in the
area o f H A B s and eutrophication, it is recognized th a t there are
fundam ental processes, trends, principles, and relationships th a t
are broadly accepted. G E O H A B w ill build on these, and w ill use
these in guiding the developm ent o f Core Research.
Several recent docum ents are highlighted here to illustrate
the com m unity consensus on the role o f eutrophication in
H A B proliferation. Each o f these efforts highlighted here was
developed w ith com m unity involvement. W h ile it is impossible
to encapsulate all o f the debate and discussion th a t occurred in
developing these consensus docum ents, nor to fully represent
all such docum ents em erging around the world, these examples
illustrate the breadth o f issues on w hich there is broad agreement.
These docum ents also consistently underscore the fact th a t an
ecosystem approach w ill be required to fully understand the
relationships betw een H A B s and eutrophication.
W ith the role o f eutrophication in the developm ent o f many H A B s
now well recognised and affirmed by various scientific and policy
groups, the specific questions for fu rth er advancem ent can now be
posed, and Core Research can be developed.
I■
M' *■ ■¡.--.iirvT«)
---------------
28
In 1999, the US N ational C enter for
C oastal O cean Science completed an
assessment o f estuarine eutrophication
(Bricker et al. 1999). This assessment,
w hich w ill be updated in 2006, was
based on results o f a survey conducted
over th e years 1992-1997 on nutrient
inputs, population projections, and
land uses. It included more th a n 138
estuaries, representing more th a n 90%
o f the estuarine surface area o f the
U nited States. A m ong th e key findings
T h e " D e a d Z o n e " ( r e d a r e a ) o f t h e G u l f o f M e x ic o . S o u r c e : N .
R a b a l a is , L U M C O N .
Gulf of Mexico, USA
Hypoxia in the Gulf of Mexico, USA, is the result of nitrogen
loading from the Mississippi River which drains significant
agricultural lands. This nitrogen leads to large algal blooms,
which, in turn, sink to the bottom and decay. The hypoxic
zone in this region in the late 1990s was twice the extent that
it was in the late 1980s. One HAB species, Pseudo-nitzschia,
has been found to be increasing in this region in direct
proportion to the increasing nitrogen loads in the Gulf of
Mississippi.
N itrate le a d in g (pM )
The average abundance (%) of the diatom Pseudo-nitzschia
in the sedimentary record as a function of the nitrate loading
in the northern Gulf of Mexico. Redrawn from Turner and
Rabalais 1991 and Parsons et al. 2002.
symptoms o f eutrophication are prevalent in US estuaries;
hum an influence on the expression o f eutrophic conditions is
substantial; and
im pairm ent to estuarine resources, and fisheries in particular,
is high.
A S y n o p sis
S e d im e n t s a n d p h y t o p l a n k t o n b l o o m , m o u t h o f t h e Y a n g t z e , E a s t
L a r g e r e d t id e s w e r e v is ib l e in t h e e a s t C h i n a S e a , 2 0 0 5 . P h o t o :
C h i n a S e a . P h o t o : N A S A V is ib l e E a r t h , v is ib l e e a r t h . n a s a . g o v .
J . L i.
China
The average number of harmful blooms (red line), in addition
to their areal extent and duration along the east coast of
China have escalated in the past tw o decades coincident with
the increasing use of synthetic fertiliser (blue bars).
ie
1970
1475
1950
1455
1990
1495
B
In M arch 2002, the International C ouncil for th e Exploration
o f the Sea (IC E S) convened a workshop in The H ague, The
N etherlands, on the linkage betw een eutrophication and its effects
on phytoplankton. Consensus was reached on the following
points:
•
There is evidence th a t anthropogenic nutrient supply to coastal
waters is leading to altered phytoplankton dynamics.
•
W h ile the underlying factors (mechanisms) and ecological
principles (e.g., dose-yield responses) apply universally, the
outcome o f th e collective phytoplankton response to nutrient
loading is often site-specific; functional group responses are
more predictable th a n species-level responses.
•
Useful models (for m anagem ent purposes) o f the effects o f
nutrification on phytoplankton mass balances and functional
group responses are attainable.
•
M an y knowledge and technical gaps exists, am ong w hich
are the need for field observations to be carried out on tim e
and space scales th a t m atch processes, ecophysiological
data in support o f models, and better understanding o f the
relationships betw een food web alterations and nutrient
enrichm ent.
2000
Redrawn from Anderson et al. 2002 and Zhou 2005.
29
A S ynopsis
In January 2003, the US Environm ental Protection Agency
sponsored a scientific “roundtable” w ith the objective o f developing
a scientific consensus on the role o f eutrophication and H A B s.
A pproxim ately 25 scientists from th e US were in attendance. Based
on keynote presentations and discussion, the following statem ents
were unanim ously adopted:
•
D egraded water quality from increased nutrient pollution
prom otes the developm ent and persistence o f many H A B s and
is one reason for their expansion in the US and the world.
•
The com position - not ju st the total quantity - o f the nutrient
pool im pacts H A B s.
•
H igh-biom ass blooms m ust have exogenous nutrients to be
sustained.
•
B oth chronic and episodic nutrient delivery prom ote H A B
development.
•
Recently developed tools and techniques are already
im proving the detection o f some H A B s, and em erging
technologies are rapidly advancing tow ard operational status
for the prediction o f H A B s and th eir toxins.
•
E xperim ental studies are critical to fu rth er the understanding
o f the role o f nutrients on H A B expression, and will
strengthen prediction and m itigation o f H A B s.
M anagem ent o f nutrient inputs to the w atershed can lead to
significant reduction in H A B s.
30
P h y t o p l a n k t o n b l o o m in G u l f o f C a l i f o r n i a . P h o t o :
NASA V
is ib l e
E a r t h , v is ib l e e a r t h . n a s a . g o v .
Gulf of California, USA
Runoff from agricultural regions has recently been associated
w ith massive blooms in the Gulf of California. These blooms
were found to occur w ithin days of fertiliser applications
(Beman et al. 2005). Total nitrogen loads from these
applications are sufficient to support these massive blooms.
For example, urea concentrations can exceed 40 pMol N L-1
following fertilisation (Glibert et al. 2006).
300
Nitrogen applied to
Agriculture in
Yaqui Valley
250
I
200
|¡
150
I
o
à
100
50
19SO
1900
1970
19S0
1990
2000
Source: International Maize and Wheat Improvement
Center (CIMMYT database).
In 2004, the Study G roup to Review Ecological Q uality Objectives
for E utrophication (S G E U T ) convened by IC E S evaluated the
linkage betw een eutrophication and H A B s in E uropean coastal
w aters (Aertebjerg and Sm ayda2004). The S G E U T report
emphasised the complexity o f the relationship betw een H A B s and
eutrophication by affirm ing th a t H A B s are an ecosystem -regulated
response and not the result o f simple, linear responses to nutrients,
being also influenced by microbial and grazer com m unities and
physical oceanographic conditions.
A S y n o p sis
P h y t o p l a n k t o n b l o o m in t h e B l a c k S e a . P h o t o : N A S A V is ib l e
E a r t h , v is ib l e e a r t h . n a s a . g o v .
Black Sea
Phytoplankton blooms in the Black Sea in the mid-1990s
increased to levels more than 20-fold higher than were
observed in the 1960s. These increases were especially
apparent during the rapid escalation of nitrogen and
phosphorus loading during the 1980s. Dinoflagellate
abundance increased 4-fold over this period, while diatom
abundance decreased.
16
7G
U
ED
u
10
SV
e
ah
£
4
20
2
10
0
0
Modified and redrawn from Oguz 2005.
1
■U
S
G
S
G
£
i
ï
1
S
In O ctober 2004, the 3rd International N itrogen Conference was
held in N anjing, C hina w ith an aim tow ard understanding the
“im pacts o f population grow th and economic developm ent on the
nitrogen cycle: consequences and m itigation at local, regional, and
global scales”. The participants o f the conference affirmed, among
other statem ents, that:
“...in many parts o f the world, significant am ounts o f reactive
nitrogen are lost to the environm ents in agricultural and
industrial production and fossil fuel com bustion. This has
lead to disturbances in the nitrogen
cycle, and has increased the probability
o f nitrogen-induced problems, such
as pollution o f freshwater, terrestrial
and coastal ecosystems, decreasing
biodiversity, and changing clim ate, and
poses a th reat to hum an health.”
In 2005, the European
E nvironm ental A gency reported th at
“E u tro p h icatio n ...is still one o f the
major environm ental problems across E urope” (www .eea.
eu.int, R eport No. 7/2005). E utrophication affects waters
from inland w ater bodies such as groundw ater, rivers and
lakes, to transitional and coastal waters and ecosystems in
open seas. They fu rth er affirmed that:
ru n o ff from agricultural activities is the m ain source of
nitrogen pollution and nitrogen loads parallel the surplus o f
nitrogen applied to large agricultural catchments;
households and industry are th e major sources o f phosphorus
pollution; and
discharges from nitrogen and phosphorus are showing
declines based on measured to reduce these inputs, but have
been larger for phosphorus w ith reduced point sources.
31
4. Priorities and Challenges for
Understanding the Relationship Between
HABs and Eutrophication
t
¡
~ È
-
,
or many years, research on HABs was
undertaken in response to specific events,
and conducted in localised areas where
specific problems occurred. Over the past decade,
enormous strides have been made internationally in
linking the global community of scientists to better
understand the factors that lead to specific blooms, their
population dynamics, and their impacts, and to do so in
a comparative framework where research questions are
B a l t i c S e a c y a n o b a c t e r ia b l o o m . P h o t o : K . K o n o n e n .
similar. In some cases, comparative studies have shown
that similar processes are controlling blooms in similar
ways. In other studies, apparently similar species occur
in various parts of the world, but they differ in growth
dynamics or expression of harmful attributes.
O f relevance to th e focus on the role o f eutrophication in H A B
proliferation, a comparative approach is highly beneficial in the
ability to compare gradients o f responses. For example, discharge
from land in Europe and A sia appears to be significantly higher
th a n in much o f the rest o f the world. These higher loads may
potentially hold the key to understanding some o f th e dynamics
o f differential H A B occurrences. A specific example is th a t o f
the colonial prym nesiophyte Phaeocystis, w hich is th o u g h t to have
proliferated in th e N o rth Sea as a result o f changing nutrient loads
and ratios from the major rivers o f the region have been modified
(Lancelot et al. 1987, 2005). In contrast, however, blooms of
Phaeocystis have only a lim ited range in the U nited States, localised
prim arily in th e G u lf o f M aine and Cape C od Bay, and are o f
significantly smaller scale and duration (A nderson et al. 2005a).
D oes th is difference reflect lower nutrient loads or different
nutrient ratios, differences in species or strains o f Phaeocystis, or
other ecological factors?
32
Key Features
fa rm in g
d eve lo pm en t
pho sp ho ru s load
w a te r tre a tm e n t plan ts
n itro g e n load
in d u stry
a tm o sp h e ric n itro g e n
tra n s p o rta tio n
Prim ary Symptom Expressions
R
high ch lo ro p h yll
X
a qu a tic biota
to x ic /h a rm fu l bloom
SAV
high dissolved oxygen
m a cro alga e bloom
high w a te r q u a lity
Secondary Symptom Expressions
« *
s h e llfis h c o n ta m in a tio n
o r die o ff
algae die o ff
fis h leave or
die o ff
lo w w a te r q u a lity
A
lo w dissolved oxygen
i
loss o f lig h t
p e n e tra tio n
a eroso lize d
to x in s
SAV loss
H ighlighted in this chapter are th e key questions th a t can and
should be studied on an international comparative basis. Examples
are provided o f detailed research questions in comparative
systems. In m ost cases, suitable sites and suitable comparative
studies are numerous; thus, the identified questions and systems
are representative but not a comprehensive review. This section
concludes by outlining several specific, but tractable, challenges
th a t should also be addressed w ith high priority.
C o n c e p t u a l d ia g r a m o f t h e p r o c e s s o f e u t r o p h ic a t io n . S o u r c e : t h e
I n t e g r a t i o n a n d A p p l i c a t i o n N e t w o r k , U n i v e r s it y o f M a r y l a n d
C e n t e r f o r E n v i r o n m e n t a l S c ie n c e , w w w . i a n . u m c e s . e d u .
Major HAB impacts in the coastal United States
9
C j« o o b # c t* rtí
0
N cnjrctoocic S fn flfisii
! '
* P*.*lylK
A
A m o « « S h e i t i i i i f e o * » n lo g
■
C i g i u t a * f n ii f o f e w m g
0
P*1*iompJe»
G Brawn T«tfe
□
A
WUtr-.ultytr i H d if r r jC ú r i
rr>h. l.w rl. rrv im iru d f t > jil.H im ijr:l
jMtuAtHvMjpUnrtfl Uh
V i r t u a l l y e v e r y c o a s t in t h e U n i t e d S t a t e s is n o w i m p a c t e d b y
HABs,
AND THE SAME IS TRUE THROUGHOUT MUCH OF THE WORLD.
S ource:
D.
A n d e r s o n , W H O I N a t i o n a l O f f ic e f o r M a r i n e
B io t o x in s a n d H a r m f u l A l g a l B l o o m s .
33
Key Q u e stio n s
n < i
□ 1'-io
■ fttO
EZÜ20-SO
■ »100
□ io « »
□ hkfwo
E l >500
Key questions to be addressed in the
understanding the ecology and
oceanography of HABs in eutrophic
systems
QUESTION 1
G l o b a l d i s t r i b u t i o n o f P r o r o c e n t r u m m i n i m u m is s h o w n ( r e d
d i a m o n d s ) s u p e r im p o s e d o n t h e g l o b a l e x p o r t m a p o f N f r o m
r iv e r s ( f r o m S e it z in g e r a n d K r o e z e 1 9 9 8 ) .
T h e h ig h e s t d e n s it y o f
OBSERVATIONS OF THIS SPECIES OCCURS IN REGIONS WHERE G LOBAL D I N
EXPORT IS PREDICTED TO BE H IG H . REPLO TTED FROM H E IL ET A L . 2 0 0 5
and
G l ib e r t a n d B u r k h o l d e r 2 0 0 6 .
Diminishing Î*, Increasing hm
increasingly
eutrophic
coastal
temperate
frontal
temperate
shallow
s h e lf
O ne o f the im portant objectives o f comparative studies on H A B s
is to understand com m onalities th a t drive plankton com m unity
structure. The concept o f “functional groups” provides a basis for
simplification in order to improve our predictive ability relative
to the dynamics o f the system. The term “functional group” (or
“life form ”) is operationally defined to mean “a non-phylogenetic
classification leading to a grouping o f organisms th a t respond in
a similar way to a syndrome o f environm ental factors” (G itay and
N oble 1997). The organisms w ithin a functional group share one
or more adaptations to those environm ental conditions (M argalef
1978).
(sp rin g )
highly
post opwelling
stra tifie d
tro p ic a!
M a r i n e p é l a g i a l h a b it a t s a s a f u n c t i o n o f l i g h t a n d n u t r i e n t f ie l d s
( S m a y d a a n d R e y n o l d s 2 0 0 1 ) . T h e s e h a b it a t s s e l e c t f o r H A B
SPECIES, FUNCTIONAL GROUPS, OR LIFE FORMS AND REFLECT THE ABILITIES
Smayda and Reynolds (2001) have provided a conceptual model
for classifying H A B dinoflagellates by functional group. They
identified nine distinct and diverse habitat types in w hich
dinoflagellates may bloom. Associated w ith each habitat type are
dinoflagellates life forms th a t ordinate on a habitat tem plate along
onshore-offshore gradients o f decreasing nutrients, reduced m ixing,
and deepening o f the euphotic zone. Several o f these functional
groups are associated w ith nutrient-rich or eutrophic waters. For
example, dinoflagellate genera, such as Prorocentrum, Phaeocystis,
Heterocapsa, Scrippsiella, Cochlodinium, Heterosigma and others,
have adaptations m aking them suitable for thriving in nutrient-rich
waters. Increasing evidence suggests th a t some o f these species also
may be increasing in their global extent.
34
OF THE SPECIES TO GROW AS PHYSICS OR BEHAVIOUR ALTER VERTICAL
DISTRIBUTIONS AND GROWTH POTENTIAL IN ALL HYDROGRAPHIC REGIMES.
A sim ilar classification based on functionality has been developed
for freshwater phytoplankton (Reynolds et al. 2002). This
conceptual model is based on tolerances and sensitivities to
a range o f physical and nutrient conditions. Some nitrogenfixing cyanobacteria species capable o f form ing blooms, such as
Cylindrospermopsis raciborskii, are able to tolerate low nitrogen
conditions, while others, such as Microcystis, appear to favour
eutrophic conditions. Such a fram ew ork provides a context for
comparative studies o f species. Sim ilar matrices w ill also need to
be developed for other H A B species.
Key Q u e stio n s
A ltered nutrient loads have been associated w ith increasing
abundance o f Pseudo-nitzschia in the northern G u lf o f M exico since
the 1950s (Parsons et al. 2002). D u rin g the same period o f tim e,
nitrogen loads have doubled, while silica availability has decreased
substantially (Turner and Rabalais 1991). This relationship has
also been observed in E uropean waters, where long-term increases
in nitrate loading parallel the increase in abundance o f th is genus
in the sedim entary record. Relatedly, in the w estern and northern
A driatic Sea, a shift from predom inantly red tide blooms to more
frequent m ucilaginous blooms occurred in the 1980s coincident
w ith phosphorus removal from detergents and expansion o f sewage
treatm ent plants (Sellner and F onda-U m ani 1999); however, cause
and effect rem ain to be determ ined as m ucilaginous events were
also recorded in the region more th an 200 years ago.
O ne o f the high-biom ass H A B species th a t has been shown to
increase in abundance following events th a t lead to runoff and
increased nutrient delivery is Prorocentrum minim um (H eil et al.
2005). This species can develop to high standing stocks and result
in harm ful im pacts on benthic habitat, including hypoxia/anoxia,
as well as on shellfish, depending on th eir life stage. Blooms
o f this species have been observed in tropical, subtropical, and
tem perate regions (H eil et al. 2005). P. minimum is one o f many
m ixotrophic species and w ill grow well when organic nutrients are
supplied (L i et al. 1996, C arlsson et al. 1998, G libert et al. 2001).
H um ic and fulvic acids from Swedish rivers increased P. minimum
intracellular nitrogen pools, cell numbers, and grow th rates
relative to cultures free o f natural organics (G ranéli et al. 1985). In
tributaries o f Chesapeake Bay, U SA , P. minim um also appears to
grow and develop into massive blooms th a t have been associated
w ith declines in submerged grasses and benthic habitat (Gallegos
and Jordan 2002), and have proven to be toxic under some grow th
conditions (W ikfors 2005). These blooms have increased in
m agnitude w ith the eutrophication o f the Chesapeake Bay, and cell
counts are now comm only more th a n an order o f m agnitude higher
th a n recorded ju st tw o decades ago. These blooms, like those in
Sweden and many other regions o f the world, appear to intensify
and expand in response to delivery o f nutrients from rainfall
events, and in particular, from organic nitrogen delivery (G libert et
A BLOO M OF THE DINOFLAGELLATE LINGULODINIUM POLYEDRA RESULTED
IN A VISIBLE RED TIDE OFF SOUTHERN C A L IF O R N IA , U S A , SUMM ER 2 0 0 5 .
P hoto: S. O h .
al. 2001, H eil et al. 2005). Through comparative studies it should
be possible to ascertain w hether these sim ilar factors are indeed
stim ulating these blooms, and w hether these blooms are increasing
in frequency globally.
Com parisons o f the physical dynamics o f the regions,
quantification o f nutrient delivery and the trophic dynamic
com position o f th e plankton at the tim e o f nutrient inputs, and the
detrim ental im pacts o f these blooms w ill be extremely valuable
in developing predictive capabilities. In addition, com parison o f
strains w ill yield insight into comparative physiology, including the
ability o f different strains to produce toxins in response to certain
environm ental factors. Suitable models are needed to explore the
interactions betw een nutrient status, physiological ability, and
other factors leading to changes in biomass.
1. Can functional groups of HABs be defined that are
2. Are there specific adaptive strategies used by HABs in
3. Can the nutritional strategies of different HAB species be
used to predict their responses to eutrophication?
4. How does intraspecific variability (strain differences) in
response to eutrophication control HAB development and
35
Key Q u e stio n s
A CROSS-ISOBATH TRANSPORT MECHANISM
FOR INITIATION OF At EXANDRtUM BLOOMS
UPWELUNG
lALTlkalr
DOWNWELUNG
I/AUtf;
MxjtJtinfj,
P h y s ic a l e n v ir o n m e n t s in t e r a c t w i t h o r g a n i s m b e h a v i o u r in
BLO O M IN IT IA T IO N , AS SHOW N HERE FOR ALEXANDRIUM BLO O M S . D U R IN G
UPW ELLING -FAVO UR ABLE W IN D S , THE PLUME TH IN S VERTICALLY A N D
EXTENDS OFFSHORE, OVERLYING THE CYSTS SEEDBEDS. ALEXANDRIUM CELLS
ARISING FROM THE CYSTS SW IM TO THE SURFACE A N D ARE TRANSPORTED
ALON G THE COAST W IT H D O W N W E LLIN G -FA V O U RABLE W IN D S . SOURCE:
population’s range and biomass are affected by physical controls
such as long-distance tran sp o rt (e.g., Franks and A nderson 1992),
accum ulation o f biomass in response to water flows and sw im m ing
behaviour (Kamykowski 1974), and the m aintenance o f suitable
environm ental conditions (including tem perature and salinity,
stratification, irradiance, and nutrient supply; W hitledge 1993).
M c G il l ic u d d y e t a l . 2 0 0 3 .
QUESTION 2
To what extent do residence time and other physical
processes impact the relationship between nutrient loading
and HAB proliferation?
O ne o f the difficulties in lin k in g nutrient loading to H A B s is
the m ultiplicity o f factors contributing to H A B species responses
to nutrient loading. A n understanding o f th e physical dynamics
o f blooms in relation to nutrient dynamics w ill help lead to an
understanding o f how bloom dynamics may differ w hen nutrient
loads are sim ilar but physical controls are different.
Physical processes are im portant at every stage o f bloom dynamics.
The initiation o f a bloom requires successful recruitm ent o f a
population into a water mass. This may result from excystment
o f resting cells during a restricted set o f suitable conditions (e.g.,
Alexandrium in the G u lf o f M aine; A nderson 1998), tran sp o rt of
cells from a source region where blooms are already established,
or response to unusual clim atic or hydrographic conditions (e.g.,
Pyrodinium bahamense in the Indo-W est Pacific; M aclean 1989).
Once a bloom is initiated, physical processes controlling bloom
tran sp o rt are o f param ount im portance. C oastal currents driven by
w ind, buoyancy, or other factors can tran sp o rt blooms hundreds
or even thousands o f kilom eters along the coast, often from
one m anagem ent area to another. U nderstanding the physical
dynamics underlying these tran sp o rt pathways is essential
to effective m anagem ent and m itigation o f H A B effects. A
36
Physical processes th a t are likely to influence the population
dynamics o f H A B species operate over a broad range o f spatial and
tem poral scales. Large-scale circulation affects the distribution o f
w ater masses and biogeographical boundaries. M any examples
may be found o f the influence o f mesoscale circulation on
H A B population dynamics. Eddies from th e deep ocean can,
for example, im pinge on slope and shelf regions, affecting the
transfer o f algae and nutrients across the shelf break. This type o f
tran sp o rt may be involved in th e delivery o f the Florida red tide
organism Karenia brevis to nearshore waters from an offshore zone
o f initiation (Steidinger et al. 1998). A lthough eddies are difficult
to resolve thro u g h sam pling at sea, they can usually be detected
thro u g h rem ote sensing o f tem perature, sea-surface height, or
ocean colour. U nderstanding o f the m ain features o f circulation
is often sufficient to devise models th a t may be used to guide
decision-m akers on the movement and developm ent o f H A B s,
although such predictions are still mostly rudim entary.
Processes at interm ediate scales result in the form ation o f
convergence zones, fronts, and upwelling. The retentive nature of
some sem i-enclosed coastal systems, such as estuaries and fjords,
can produce long residence tim es leading to prolonged suitable
periods for cells to thrive (Cem bella et al. 2005). The im portance of
fronts in bloom developm ent, including H A B s, is now recognised
and included in some m odelling efforts (Franks 1992). A linkage
has been dem onstrated, for example, betw een tidally generated
fronts and the sites o f massive blooms o f the toxic dinoflagellate
Gyrodinium aureolum (=Karenia mikimotoi) in the N o rth Sea
(H olligan 1979). The typical p attern is th a t o f a high surface
concentration o f cells at th e frontal convergence, contiguous w ith a
subsurface chlorophyll m axim um th a t follows the sloping interface
Key Q u e stio n s
betw een the tw o water masses beneath th e stratified side o f the
front. The signature o f the chlorophyll m axim um , sometimes
visible as a “red tide”, may be 1-30 km wide. Chlorophyll
concentrations are generally lower and much more uniform on the
w ell-m ixed side o f the front. The significance o f th is differential
biomass accum ulation is best understood when movement o f the
front and its associated cells brings toxic dinoflagellate populations
into contact w ith fish and other susceptible resources, resulting in
massive m ortalities. This is an example where physical-biological
coupling results in biomass accum ulation, and larger-scale
advective m echanism s interact synergistically in a way th a t results
in harm ful effects.
The im portance o f small-scale physical processes in H A B
developm ent is observed in the layering o f the physical, chemical,
and biological environm ent in stratified coastal systems. O ff
the French coast, for example, a th in layer o f dinoflagellates,
including the H A B species Dinophysis cf. acuminata, has been
observed in the region o f the therm ocline (G entien et al. 1995,
2005). The same pattern is found for Dinophysis norvegica in the
Baltic Sea, where a 1-2 m th ick layer w ith up to 80 000 cells-1 is
usually situated betw een 20-25 m depth, where light is less th an
1% (Gisselsson et al. 2002). Several H A B species are well know n
for th eir ability to form these th in , subsurface layers o f uncertain
cause and unknow n persistence, at scales as small as 10 cm in the
vertical and 10-1000 km in the horizontal (Gisselsson et al. 2002).
O ne explanation is th a t these layers result from the stretching
o f horizontal inhom ogeneities by the vertical shear o f horizontal
currents. This produces an environm ent potentially favouring
motile organisms th a t can m aintain th eir position in th is layer or
organisms able to regulate th eir buoyancy. A ny comprehensive
study o f H A B s, including studies focussing on nutrient controls,
should incorporate an understanding o f the physical conditions
th a t can lead to cell aggregation and dispersion.
L E F T : D in o p h y s is a c u m in a t a . P h o t o : w w w . s d n - w e b . d e .
R I G H T : D i n o p h y s i s b l o o m in c o a s t a l N o r w a y . P h o t o :
H a v f o r s k n in g s in s titu t te t, I n s t it u t e o f M a r in e R e s e a rc h , w w w .
a lg e in fo . im r .n o .
The need to understand physical dynamics has further im portance
in understanding the relationship w ith nutrients. For example, the
responses o f phytoplankton to fluctuating lig h t (due to sw im m ing
behaviour and turbulence) are not the same as responses to the
average exposure. There is cause to suspect th a t synergistic events
may prom ote toxicity above th a t w hich would be expected from
knowledge o f th e im pact o f individual processes (Flynn 2002).
Similarly, for nutrient uptake, the kinetics o f uptake measured
under steady-state conditions may not apply w hen cells are exposed
to highly variable nutrient environm ents, w hether from changes
in vertical nutrient structure or from exposure to ephemeral
patches o f nutrients (e.g., G oldm an and G lib ert 1983). Thus,
there are many needs for understanding the relationships between
physical environm ents and the physiological responses o f the cells.
Com parisons am ong sim ilar species in different hydrographic
regim es, as well as comparisons across species in similar
hydrographic regim es, w ill be useful in th is regard.
Examples of Relevant Detailed Questions
1. Do residence time and physical processes impact the
likelihood for different species to bloom under eutrophic
conditions in different ways or at different stages in the life
cycle?
2. What are the physical factors that contribute to the
persistence of high-biomass blooms in eutrophic systems?
3. To what extent do systems w ith the same indigenous
species and nutrient load develop similar blooms when
physical processes differ?
4. How do physical processes control the physiological
responses of different species to light and nutrients?
37
Key Q u e stio n s
+
W ater
MPB
clarity
Biom ass
Nutrient
av ailab ility
Brown tide
biomoss
MPB
Productivity
MPB
Biomass
■=>
%
Browntide
productivity
Water
N u trient
Brawn tide
clarity
availability
productivity
n MPB
s i ^
Productivity
G row n tid e
bio m ass
C o n c e p t u a l r e l a t io n s h i p s b e t w e e n m i c r o p h y t o b e n t h o s
(MPB)
and
QUESTION 3
blo o m s of
How do feedbacks and interactions between nutrients and
the planktonic, microbial food webs impact HABs and their
detrimental effects?
UPPER PANEL, A BENTHIC DO M IN ATE D STATE W IL L LEAD TO LO W BROW N TIDE
A u r e o c o c c u s a n o p h a g e f f e r e n s ( b r o w n t id e ) . N o t e in t h e
BIO M ASS, W HILE IN THE LOWER PANEL, PELAGIC NUTR IEN T- ENRICHMENT
CAN LEAD TO HIGH BROWN TIDE BIO M AS S. M O D IF IE D A N D REDRAWN FROM
M a c I ntyre et a l . 2 0 0 5 .
N utrient enrichm ent can stim ulate H A B s not only directly by th eir
support o f increased biomass, but indirectly, in more subtle but
significant ways over the long term - for example, by increasing
hypoxia th at, in tu rn , elim inates filter-feeding shellfish th a t
w ould have consum ed H A B s but th a t can no longer survive in
the habitat (Burkholder 2001, G libert et al. 2005, Smayda 2005).
Similarly, im pacts o f nutrients may be rem oved in tim e and space
from the nutrient source as nutrients are consum ed, recycled, and
transform ed, leading to complex - and often indirect - interactions
betw een nutrients and H A B s (G libert and Burkholder 2006). In
addition, bacterial interactions are often o f critical im portance in
the developm ent o f toxins w ithin some H A B species, and these
interactions may occur differently under varying nutrient regimes.
H arm fu l algae do not exist in isolation in natural ecosystems,
and are influenced by interactions betw een individual cells o f the
same and other members o f th e planktonic comm unity. Food-web
interactions have a profound effect on the population dynamics
o f H A B species. Processes such as com petition and grazing can
affect the net grow th rates o f algae in nature. O n the other hand,
grazing may also increase nutrient regeneration, thus altering
the availability o f some nutrient forms for the algae to consume
(G libert 1998, M itra and Flynn 2006).
Viruses are now know n to have significant im pacts on the
dynamics o f m arine com m unities and some have been found to
infect algae and have been im plicated in the demise o f red or brown
tide blooms (F uhrm an and Suttle 1993). Likew ise, bacteria play
an im portant role in controlling many H A B s and regulating th eir
im pacts, including their toxicity. Bacteria may also interact w ith
H A B s in a positive m anner by stim ulating th eir grow th (Fistarol
38
et al. 2004a). Unique microbial com m unities are often associated
w ith nutrient-rich systems, affecting internal nutrient cycling.
C yanobacteria, in particular, establish m utually beneficial
consortia, by chem otactically attracting and supporting m icro­
organisms involved in nutrient cycling and the production of
grow th factors (Paerl and M illie 1996). A different type o f bacterial
interaction w ith H A B species was described by Bates et al. (1995),
who showed th a t th e toxicity o f the diatom Pseudo-nitzschia was
dram atically enhanced by the presence o f bacteria in laboratory
cultures. The extent to w hich any o f th e above interactions occur
in natural waters, and affect H A B dynamics and/or toxicity, is not
know n, representing an im p o rtan t line o f inquiry.
The effects o f nutrient inputs on H A B s are not always direct;
there are indirect pathways by w hich nutrients can influence the
developm ent o f H A B s. For example, nutrients may be consum ed
and/or transform ed from one form to another, thereby increasing
th eir bioavailability for H A B species. O n a seasonal scale, in
estuarine systems such as th e Chesapeake Bay, U SA , nutrient
input in the spring is delivered largely in the form o f nitrate and is
rapidly assim ilated by diatom s w hich, in tu rn , sink and decompose.
Subsequently, during the w arm er sum m er m onths, nitrogen
is released via sedim ent processes in the form o f am m onium ,
w hich th en supports an assemblage dom inated by flagellates,
including dinoflagellates (M alone 1992, G libert et al. 1995). The
shallow, brackish Baltic Sea is characterised by efficient cycling o f
phosphorus, coupled w ith effective removal o f nitrogen, leading
to a prevalence o f a low N :P ratio. These conditions are especially
favourable for nitrogen-fixing cyanobacteria. Furtherm ore,
cyanobacteria are favoured in conditions where anoxia in the
bottom layer leads to a release o f chemically bound phosphorus
Key Q u e stio n s
P lan ktivorous fish
C o p ep o d s
M icro zoo plan kto n
P hytoplankton
from sediments; release o f phosphorus from th is reservoir may
prolong the harm ful consequences o f anthropogenic loading for
years or decades after reductions in phosphorus input into the
system (C arm en and W u lff 1989).
C o n c e p t u a l d i a g r a m o f t o p - d o w n c o n t r o l a n d e f f e c t o f t r o p h ic
CASCADES ON SM ALL A N D LARGE CELL-SIZE P H Y TO PLA N K TO N . O n THE
LEFT, PROLIFERATION OF BAITFISH RESULTING FROM O VER-FISHING OF TOP
PREDATORS LEADS TO BLOO MS OF LARGE DINOFLAGELLATES (CIRCLED).
A l t e r n a t iv e l y , o n t h e r ig h t , r e m o v a l o f s m a l l f is h c a n l e a d t o
O n shorter tim e scales, nutrients may be taken up by a particular
species in one form and released in another form by th e same
organism or by its grazer. The cyanobacterium Trichodesmium,
w hich forms massive blooms in tropical and subtropical waters,
derives its nitrogen via the fixation o f N r However, much o f this
nitrogen is rapidly released as am m onium and dissolved organic
nitrogen (Karl et al. 1992, G libert and B ronk 1994, G libert and
O ’N eil 1999). This released nitrogen is therefore available to
support the grow th o f other microbial populations th a t cannot
otherwise derive their required nitrogen in nutrient-im poverished
waters. N um erous consortial associations involving other nitrogenfixing cyanobacterial bloom taxa (Anabaena, Aphanizomenon,
Nodularia) and bacterial epiphytes have been shown to lead to
enhanced grow th o f cyanobacterial “hosts” (Paerl 1988, Paerl and
Pinckney 1996). Relationships betw een nutrient inputs, and the
C o m p a ris o n o f th e a m b ie n t n u tr ie n t
c o n c e n tr a tio n in s id e a n d o u ts id e a
BLOO MS OF S M ALL PH YTO PLANKTO N (CIRCLED) SUCH AS BROW N TIDE.
S o u r c e : D . S t o e c k e r a n d t h e I n t e g r a t io n a n d A p p l ic a t io n
N e t w o r k , U n i v e r s it y o f M a r y l a n d C e n t e r f o r E n v i r o n m e n t a l
S c ie n c e , w w w . i a n . u m c e s . e d u .
various processes by w hich nutrients are recycled and transform ed
are im portant for understanding H A B grow th strategies.
It is highly likely th a t a com bination o f increases in nutrient
resources and relaxation in grazing together contribute to both
th e frequency and intensity o f H A B events. E utrophication alters
top-dow n control as well as providing bottom -up nutrient support
for blooms. T op-dow n control o f m icrozooplankton is particularly
im p o rtan t as predation on the m icrozooplankton com m unity
may release H A B species from grazing control. Trophic cascades,
alterations in benthic-pelagic coupling, and interactions betw een
all com ponents o f th e microbial com m unities need to be better
understood on comparative bases.
d e n s e s u rfa c e b lo o m o f T ric h o d e sm iu m
(see p h o to ). D in o fla g e lla te s w e r e
s ig n ific a n tly m o r e a b u n d a n t in th e
E x a m p le s o f R e le v a n t D e t a ile d Q u e s tio n s
p la n k to n c o m m u n ity in s id e th a n
o u ts id e , w h ile d ia to m s w e r e m o r e
a b u n d a n t o u ts id e th a n in s id e th e
Tr i c h o d e s m i u m
b lo o m . F ro m G lib e r t a n d O 'N e il 1 9 9 9 .
b lo o m . P h o to :
P. G l i b e r t .
Inside Bloom
Outside Bloom
NH4 (pM)
7.0
1.4
P04(pM)
1.2
0.2
DON (pM)
10.3
6.9
Dinoflagellates
74%
54%
Diatoms
26%
46%
1. What are the roles of bacteria and viruses in growth
dynamics and impacts of HAB species in eutrophic
environments?
2. What is the impact of eutrophication on the quality of
Zooplankton food and how does that affect grazing
activity?
3. Do HABs uniquely alter trophic interactions through their
toxin production?
4. To what extent do bacterial interactions w ith HABs lead to
toxin production that is greater in eutrophic waters?
5. How does eutrophication impact the production of
allelopathic chemicals?
39
Key Q u e stio n s
T h is f is h f a r m in t h e E a s t C h i n a S e a w a s s e v e r e l y i m p a c t e d b y
In t h e
HABs
ACCIDENTALLY INTRODUCED V IA THE BALLAST WATER OF SHIPS TO THE B L A C K
in
200 5.
P hoto:
J. Li.
e a r l y 1 9 8 0 s , t h e R a in b o w J e l l y , M n e m i o p s i s l e id y i , w a s
S e a w h e r e it h a d a c a t a s t r o p h i c e f f e c t o n t h e e n t ir e e c o s y s t e m .
P hoto:
L.
K l is s u r o v , B l a c k S e a P h o t o G a l l e r y .
QUESTION 4
Do anthropogenic alterations of the food web, including
overfishing and aquaculture activities, synergistically
interact w ith nutrients to favour HABs?
Global changes in trophic structure o f nearshore habitats are
occurring coincident w ith global changes in nutrient loading.
A ltered grazing structure, for example, has occurred from both
overfishing, as well as from the intensification o f aquaculture
activities throughout th e world. The dram atic decrease o f
im portant comm ercial fisheries in many parts o f the world may
interact synergistically to prom ote H A B s. Studies in both
lake and estuarine waters have shown th a t reductions in large
piscivorous fish leads to a trophic cascade, whereby an increase
in the smaller piscivorous fish is subsequently noted, w hich then
exerts strong predation control on Zooplankton, thereby reducing
their biomass and thus increasing th e biomass o f phytoplankton
(A ndersson et al. 1978, C arpenter et al. 1985). In th e Black Sea,
for example, over-fishing has led to a virtual disappearance o f
the large comm ercial fish, and as a consequence there has been
a dram atic increase in the predatory ctenophore Mnemiopsis
leidyi, a disruption o f the pelagic food web, and increases in
H A B s (D askalov 2002, L ancelot et al. 2002, Kideys et al. 2005)
Similarly, in N arragansett Bay, U SA , recent evidence suggests th a t
H A B s have increased as M . leidyi has become more abundant in
th a t system, also decreasing th e Zooplankton consumers o f these
H A B s (Sullivan et al. 2001).
The synergistic im pact o f trophic cascades and nutrient loading has
recently been shown by G ranéli and T urner (2002). They observed,
in mesocosms experim ents, th a t by m anipulating th e food web
through th e introduction o f jellyfish, phytoplankton biomass
increased w ithout supplemental nutrients. O n the other hand,
when nutrients were also added, the biomass o f phytoplankton, and
in particular, the biomass o f H A B species, increased significantly.
40
W h ile control o f phytoplankton thro u g h Zooplankton grazing
has been studied for a long tim e, there are still im p o rtan t gaps
in our knowledge th a t seriously hinder our ability to model the
interaction correctly (M itra and Flynn 2005) In particular, there
are insufficient data for the grazing o f phytoplankton o f different
nutritional status; not only does this affect our understanding
o f the grazing o f no n -H A B species (Jones and Flynn 2005),
but th is issue is likely to be o f even greater im portance when
considering the palatability o f H A B species whose toxicity varies
w ith nutrient availability. H ence, it is now becom ing increasingly
recognized th a t many H A B species are not efficiently grazed.
M orphological features, poor nutritional quality, as well as
intracellular or extracellular toxins or other bioactive com pounds,
may act as feeding deterrents (Verity and Smetacek 1996, T urner
and Tester 1997). A variable susceptibility o f toxic algae to
grazers is considered to reflect varying toxin levels, depending
on algal grow th condition (Turner and Tester 1997, T urner et al.
1998). F urtherm ore, increasing as well as decreasing inhibition
o f Zooplankton feeding by H A B species has been observed under
both nitrogen and phosphorus lim itation (Nielsen et al. 1990,
G ranéli and Johansson 2003a). Thus, the nutrient state o f the algae
may be o f critical im portance in controlling th eir susceptibility to
grazing. C orroborating these findings is the fact th a t for many
H A B species the toxicity increases when they are grow n under
nutrient-unbalanced conditions (G ranéli et al. 1998). The idea th at
changes in higher levels o f the food web facilitate the success of
H A B species by decreasing th eir grazers, and, thro u g h alterations
o f the nutrient pool, fu rth er decrease th eir susceptibility to grazing
by altering their toxin content, requires much more study.
G razing control o f H A B s can also depend on the population
density o f the harm ful algae, as dem onstrated for th e brow n tides
in N arragansett Bay, U SA , where suppression o f grazing occurs
above a threshold concentration (Tracey 1988). A threshold
effect may also occur if the daily production o f new harm ful cells
Key Q u e stio n s
becomes large enough to saturate the ingestion response o f the
grazers and the ability o f grazers to increase th eir populations.
In th a t case, population grow th can accelerate dram atically - if
sufficient nutrients are available to support grow th (D onaghay
1988). There is, however, little quantitative inform ation on how the
nature o f the grazer response influences the tim in g , m agnitude,
and duration o f H A B s, and for those studies where such
inform ation is available, alm ost n othing is know n about w hether
these responses would change under altered nutrient regimes.
M odel param etrisation o f these effects is thus in very early stages
o f development. However, initial m odelling studies suggest th a t
the links betw een nutrient status, toxicity, poor grazing, removal
o f no n-H A B species, and establishm ent o f many H A B s may be
driven by a positive feedback loop (M itra and Flynn 2006).
The structure o f grazing com m unities also has been altered
significantly through th e developm ent o f large aquaculture
facilities. A n example o f the association betw een fish farm ing
operations and H A B s comes from Norway. Up to the 1970s,
harm ful algal blooms were not considered a major th reat to the
m arine or coastal environm ent o f Norway. Single episodic events
o f mussel toxicity and m ortality o f w ild biota were recorded along
the N orw egian coast, but these episodes did not attract any wide
public attention or lead to any m anagem ent actions. Through the
1970s, several fish farm s were established along the coast, and
since 1980, the production o f the N orw egian aquaculture industry
grew significantly from a few thousand tonnes to ~500,000 tonnes
o f salmon and tro u t in 2001, and N orw ay’s emergence as the
w orld’s largest exporter o f A tlantic salmon. In parallel w ith this
developm ent, H A B s emerged as a significant problem. In 1981,
a large bloom o f th e dinoflagellate Gyrodinium aureolum caused
significant m ortality o f farm ed salmon and economic losses to fish
farmers. N ew blooms o f Gyrodinium followed, and during the
1980s, other phytoplankton species bloomed to cause additional
problems, including Dinophysis spp. in 1984, Chrysochromulina
polylepis in 1988, recurrent blooms o f Prymnesium since 1989,
Chrysochromulina leadbeateri In 1991, and Chattonella m 1998,
2000, and 2001. It is, o f course, incorrect to attribute these
outbreaks solely to nutrient inputs from fish farm s, but some
linkage seems probable.
T h e s e a q u a c u l t u r e f a c il it ie s i n K u w a i t h a v e o f t e n b e e n i m p a c t e d b y
HABs.
P h o t o : P. G l ib e r t .
E nrichm ent o f nutrients from aquaculture activities has also been
associated w ith outbreaks o f pathogens th a t synergistically interact
w ith H A B s to alter fish health. For example, in Kuwait, a recent
massive fish m ortality event, attributed to an outbreak o f the
pathogenic bacterium Streptococcus agalactiae'was also functionally
related to an outbreak o f PSP-producing dinoflagellates (Evans
et al. 2002, G libert et al. 2002). It was suggested th a t as massive
numbers o f fish died, nutrient release led to conditions favourable
for the dinoflagellate outbreak.
There is much th a t can be learned from comparative systems where
major alterations o f food webs have occurred through over-fishing
or over-stocking. A s new markets and regions are developing
intensive aquaculture operations, there are also opportunities for
gaining knowledge regarding the potential for increased H A B
proliferation from comparisons w ith long-established regions.
Examples of Relevant Detailed Questions
1. Under what conditions does overfishing lead to trophic
cascades that may synergistically interact w ith nutrient
availability to promote HABs?
2. Does nutrient loading uniquely alter HAB toxin production
leading to grazing alterations?
3. Is nutrient enrichment associated with both fish farming
and shellfish farming, from feed additives and nutrient
regeneration, correlated w ith HAB proliferation, and
are there unique species that develop under specific
aquaculture nutrient regimes?
41
Key Q u e stio n s
&0
7 ,0
LO
0.0
c
’f
O'
M o r e a n d m o r e v e h ic l e s , a s w e l l a s v e h ic l e s w i t h p o o r g a s
ECONOMY, ARE CONTRIBUTING TO
NOX
EMISSIONS. P H O T O : P . G LIB ER T.
•r.
o-
O'.
O'
C h a n g e in U S a t m o s p h e r i c N O x e m is s io n s f r o m 1 9 4 0 t o 2 0 0 0 .
S o u r c e: H o w a r t h et a l . 2 0 0 2 b .
QUESTION 5
How do anthropogenic changes in land use, agricultural use
of fertiliser, NOx emissions from vehicles, and global changes
inland cover affect the delivery of nutrients to coastal waters
and the resulting incidence of HABs?
A s described earlier in this report, hum an activities have altered
the nutrient regimes o f coastal waters tremendously, prim arily as a
result o f increased applications o f synthetic fertilisers. Population
grow th and developm ent, and th e production o f food (crop and
anim al production systems) result in dram atic alteration o f the
landscape as well as large sewage inputs, and increased runoff
from land. Increased nutrient inputs to enclosed and nearshore
ecosystems have resulted in w idespread coastal eutrophication
throughout Europe, Asia, and th e U nited States. The production
and consum ption o f energy also results in increased atm ospheric
inputs from N O x emissions, w hich can th en lead to increased
nitrogen deposition. In freshwater reservoirs, increased prim ary
production has been correlated w ith the proportion o f increased
agricultural land in the w atershed (Knoll et al. 2003). C om parisons
o f nutrients delivered from pristine, urban or agricultural land uses
are sorely needed. Similarly, little is know n about comparative
nutrient loading from systems undergoing rapid deforestation
and/or rapid urbanisation. O f the nitrogen th a t hum ans p u t into
the landscape, much is also denitrified. A better understanding
o f the fluxes from land to the atm osphere from denitrification,
how they change w ith climatic variations, and how they may be
altered as landscape is altered, is fundam entally im p o rtan t to our
understanding o f nutrient delivery to coastal waters (H o w arth et
al. 2006).
Y
I 13»
B
I -t»
I
*
HÚ
BOM
N ii Af r t m e w n f c N In p u t, per A n . [ Da
“*j
T h e r e l a t io n s h i p b e t w e e n h u m a n in p u t s o f N a n d r iv e r in e N e x p o r t
FOR M AJO R RIVERINE A N D COASTAL REGIONS OF THE N O R T H A T L A N T IC
O c e a n . S o u r ce: H o w ar th et a l . 1 9 9 6 .
M a n - m a d e c a n a l s r e s t r ic t f l o w , r e d u c e c ir c u l a t i o n , a n d in c r e a s e
SUSCEPTIBILITY OF THESE SYSTEMS TO BLOO MS FROM ELEVATED NUTRIENT
loads.
42
'V
P h o t o : w w w .w e n e e d a v a c a t i o n . c o m .
Key Q u e stio n s
In
F l o r id a ,
USA,
s o m e w a t e r f l o w is u n d e r g a t e d c o n t r o l .
T here
ARE O NG O IN G RESTORATION EFFORTS TO RETURN TO SURFACE FLOW,
POTENTIALLY ALTERING THE FORMS A N D AM O U N T S OF NUTRIENTS TO BE
DELIVERED TO THE COAST. P H O T O : E v E R G L A D E S /F l O R ID A
Bay W ATE R S H ED
I n C h in a , t h e T h r e e G o r g e s D a m
o n the
Y a n g t z e R iv e r , s c h e d u l e d
FOR CO M PLETIO N BY 2 0 0 9 , W IL L BE THE LARGEST HYDROELECTRIC D A M
IN THE W O R LD .
It W IL L
SIGNIFICANTLY ALTER THE DO W NSTREAM FLOW OF
NUTRIENTS. P H O T O : W W W .A F TE R D R E A M S .C O M .
M a n a g e m e n t , w w w .s f w m d .g o v .
Large-scale hum an alteration o f coastlines or inland waters also
need to be assessed for th eir effect on nutrient enrichm ent and
supply. For example, sem i-enclosed harbours and extensive
housing developm ents along artificial canals are now commonplace
world-wide, from the C atalan coast o f Spain to the east coasts o f
the U nited States and A ustralia. Reduced circulation w ithin these
harbours has been associated w ith recurrent blooms. In South
C arolina, U SA , numerous types o f H A B s have been frequently
observed in coastal detention ponds used for storm w ater control in
housing developm ents and go lf courses (Lew itus et al. 2003). These
brackish, shallow, low-flow environm ents are depositional sites
for nonpoint source pollutants, prim arily fertiliser nutrients from
intensive landscape m aintenance and tu r f managem ent. Because
these ponds exchange w ith tid al creeks, they are sources for H A B
dispersion into adjacent estuaries.
M ajor engineering projects are also projected to have im pacts
on nutrient delivery and booms. E stim ates, for example, o f the
potential eutrophication im pact o f the Three Gorges D am Project
o f the C hangjiang (Yangtze) River, C hina, suggest th a t the
nitrogen to phosphorus ratio may be significantly altered so as to
yield a shift in ecosystem structure and the developm ent o f anoxia
(Z hang et al. 1999). The im pending restoration o f surface water
flow through the Everglades in Florida, U SA , a project o f decadal
tim e scale, is expected to have major im pacts on nutrient delivery
to Florida Bay. U nderstanding the im pact o f varying nutrient
quality as well as quantity is im portant in understanding the type
o f phytoplankton bloom th a t may develop (e.g., cyanobacteria vs.
diatom ; G libert et al. 2004). A lternatively or additionally, some
fundam ental change in seagrass processes and the entire benthic
com m unity may be diverting recycled nutrients from sedim ent
pools to the overlying water colum n, fueling phytoplankton
grow th.
Spatially explicit, em pirical models have previously been developed
to quantify global nutrient export to the coastal zone as a function
o f w atershed characteristics (D u m o n t et al. 2005, H arrison et
al. 2005, Seitzinger et al. 2005a). Such models take into account
w atershed characteristics including freshwater runoff, land use,
atm ospheric deposition, hum an population, fertiliser use, and
anim al production am ong other factors. These types o f models
need to be coupled w ith long-term records o f H A B occurrences.
Finally, the relationships betw een nutrient delivery via the range
o f mechanism s described above and H A B developm ent also must
be understood in term s o f the physics o f th e water body receiving
th e nutrients. Equivalent nutrient inputs to different systems may
have differential effects on H A B developm ent due to differences in
ecosystem structure and function.
Examples of Relevant Detailed Questions
1. To what extent do similar land-use patterns lead to similar
nutrient discharges (in quantity and quality) and similar
HAB outbreaks?
2. Can long-term trends in nutrient loadings be correlated
w ith changes in HAB bloom patterns and dynamics?
3. What is the likelihood for long-term ecosystem restoration
projects to alter nutrient delivery in such a way as to
increase or decrease the frequency of HAB outbreaks?
4. How do nutrient transformation processes such as
denitrification vary w ith changes in nutrient loading to
the land and other landscape changes, and how do these
processes affect nutrient availability for HABs?
43
Key Q u e stio n s
Pro-lsabfll
PoBL-lsaÍMl
DMeranea between
SfipWfflbe* 11. 2003
Seplcm bM 24. 20Ö3
pro- and poil-lsab cl
Chi j
(mg m *1-
M
ia
I
io
Mí
*
6
4
2
0
*65
mo
longiLutíe ("WJ
*6 5
*6 0
Longitude ("WJ
76 5
*60
Longrtude i ' W )
S h o r t - t e r m n u t r i e n t l o a d i n g , s u c h a s o c c u r r e d f o l l o w in g
QUESTION 6
H u r r ic a n e I s a b e l w h i c h s t r u c k t h e C h e s a p e a k e B a y r e g io n , U S A , in
Do climate change and climate variability have impacts on
ecosystems that augment the impacts of eutrophication in
the formation of HABs?
2 0 0 3 , LED TO LARGE A LG AL BLOO MS W IT H IN DAYS. SO URCE: D . M lL L E R
In order to assess the extent to w hich nutrients and/or
eutrophication may be an im portant causative factor o f specific
blooms, the role o f interacting or confounding factors m ust also
be considered. C lim ate ultim ately controls th e fundam ental
param étrés relating to algal grow th, from water tem perature to
nutrients, and from precipitation and ru n o ff to light. Clim ate
change and climate variability can cause changes in species
composition, trophic structure, and function o f marine ecosystems.
C lim ate change is the long-term alteration in global and/or
regional w eather due to increasing concentrations o f greenhouse
gases and aerosols th a t have altered the radiation balance o f the
E arth. C lim ate variability, on the other hand, is the natural
variation in the im pact o f solar variation on clim ate, including
periodic E l N iño-S outhern O scillation (E N SO ) phenom enon,
the N o rth A tlantic O scillation (N A O ), and th e Pacific Decadal
O scillation (PD O ).
N utrient supply is linked to freshwater input (e.g., Caraco 1995,
Vitousik et al. 1997) th a t, in tu rn , is driven by regional climate
variability (Najjar 1999, M iller et al. 2005, Burkholder et al.
2006, H ow arth et al. 2006). Freshwater input determ ines, to a
large extent, the spring chlorophyll a m axim um in systems such
as Chesapeake Bay, U SA , by delivering nutrients (H ard in g 1994,
M alone et al. 1996, Kemp et al. 2005). Freshwater input also plays
a role in the physical tran sp o rt o f phytoplankton species, such as
the H A B species Prorocentrum minimum (Tyler and Seliger 1978),
blooms o f w hich have been shown world-wide to be associated w ith
freshwater inputs and associated nutrients (Silva 1985, G ranéli
and M oreira 1990, Stonik 1995, G rzebyk and Berland 1996,
44
ET A L . 2 0 0 6 .
G libert et al. 2001, Springer et al. 2005). Inter-annual variability
is also im portant, however, affecting the tim in g o f freshwater
flow, residence tim es, and the m agnitude and tim in g o f blooms,
including H A B s. In the case o f brow n tide in th e Peconic Estuary,
U SA , for example, a paucity o f inorganic nitrogen addition via
groundw ater during dry years has been shown to stim ulate the
grow th o f the brow n tide organism , Aureococcus anophagefferens
(LaR oche et al. 1997, N uzzi and W aters 2004) w hich can utilize
D O N resulting from th e partial m ineralisation o f the previous
year’s algal grow th or from the same year’s spring bloom (Gobler
and Sañudo-W ilhelm y 2001). M ajor climatological events, such as
strong storms or hurricanes, also affect estuarine conditions during
short tim e periods. A s examples, H urricane Isabel in 2003 caused
a large phytoplankton bloom to develop in Chesapeake Bay, U SA,
w ithin days (M iller et al. 2005), as did H urricanes Charley and
W ilm a off the Florida coast (H eil et al., unpub. data).
A s climate w arms, one predicted scenario is for alteration in
rainfall, leading to increased riverine discharge. Such an increase
may lead to lowered salinity, increased abundance o f taxa th a t
proliferate in lower salinity waters, including freshwater bloomform ing cyanobacteria. W ith increased discharge, such species
may also be carried fu rth er seaward, leading to potential exposure
o f new regions to toxin-producing cyanobacterial blooms.
A dditionally, buoyant plumes could extend m uch fu rth er off the
coast, selecting for m igrating taxa such as dinoflagellates, w hich
recur in these coastal features (Sellner and Fonda-U m ani 1999).
A lternatively, for systems w ith declining riverine discharge, more
stenohaline taxa could potentially move fu rth er up estuaries,
thereby exposing larger portions o f upper basins to more saline
H A B taxa such as Dinophysis, Karenia, and Alexandrium.
Key Q u e stio n s
SH2¿
1 -y e a r
running m e a n o f S [ - Q J
%\NAO\
HAB®
year (20th Century)
The current ecological paradigm suggests th a t an ecosystem
does not exist in a unique, stable equilibrium state, but rather
can easily be shifted to a new state by non-linear responses to
physical forcings, such as those associated w ith climate change or
variability. Biological responses are non-linear, complex m ixtures
o f physiology, behaviour, life history, and physical redistribution.
A major question is w hether changes in climate synergistically
interact w ith changes in nutrient loads to lead to increased
frequency o f H A B s.
P o s s ib l e l o n g - t e r m r e l a t i o n s h i p b e t w e e n c l i m a t e v a r i a b i l i t y a n d
P a r a l y t i c S h e l l f i s h P o is o n i n g e v e n t s c a u s e d b y G y m n o d i n i u m
CATENATUM IN THE G A L IC IA N R iA B a IX A S ( N W IBERIAN P E N IN S U L A ). S [ Q X] A N D S [ N A O ] ARE DE-SEASONALISED CU M ULATIVE SUMS OF OFFSHORE
E k m a n t r a n s p o r t ( - Q x) a n d t h e N o r t h A t l a n t i c O s c i l l a t io n in d e x
( N A O ) o v e r t h e p e r io d 1 9 8 1 - 1 9 9 8 . T h e s t r a i g h t r e d l in e in d ic a t e s
YEARS OF DETECTION OF
G. CATENATUM ASSOCIATION
W ITH (THICK LINE) OR
ABSENCE FROM (TH IN LINE) THE DETECTION OF P S P TOXINS IN SHELLFISH.
A POSITIVE TREND IN S [ N A O ] INDICATES TRANSITIO N TO U PW ELLING FAVOURABLE PERIODS. A NEGATIVE TREND IN S [ N A O ] INDICATES
C lim ate changes are also resulting in global variations in
tem perature. W hile average global changes may be relatively small,
effects o f climate w arm ing vary widely by region. Tem perature
is a fundam ental regulator o f physiological processes, affecting
the activity o f specific enzymes and th e cues for various life cycle
events, such as excystment. Tem perature also regulates abundance
and activity o f predators. The extent to w hich these physiological
controls and synergistic relationships w ith other com ponents of
the food web are regulated by tem perature, is far from understood.
O ne example o f such interactions is th a t o f Heterocapsa triquetra,
w hich blooms during w inter in N o rth C arolina, U SA (Litaker and
Tester 2005). O n a physiological level, H. triquetra is favoured
under conditions o f w arm tem peratures and high light. Yet, due
to tem perature control on its grazer, it tends to bloom at cooler
tem peratures when grazers are kept in check. I f w inters become
warm er, the tim ing o f such blooms may be altered.
TRANSITIO N TO DO W NW ELLIN G -FA VO U RA BLE PERIODS. P S P OUTBREAKS
CAUSED BY
G. CATENATUM WERE
MORE FREQUENT A N D INTENSE DURING
THE TRANSITIO N PERIOD ( 1 9 8 0 s TO 1 9 9 0 s ) FROM D O W N W E LLIN G - TO
U P W ELLIN G -FAVO U RABLE CO N D ITIO N S . SO URCE: A lV A R E Z -S a L G A D O ET AL.
2003.
Examples of Relevant Detailed Questions
1. Whatare the chemical paramétrés that are likely to
change due to climate and how might they impact HAB
proliferation?
2. How do either small or large changes in temperature
impact cellular physiology favouring HABs?
3. Do ENSO and other large-scale physical forcings have
impacts on HABs?
4. How do climate variability and changes impact river flow
and the associated transport of nutrients leading to HABs?
45
Key Q u e stio n s
A B a l t i c S e a b l o o m , p o s s i b ly N o d u l a r i a , J u l y 2 0 0 5 . P h o t o : J .
D e s c lo itr e s , M O D I S L R R T , N A S A G S F C .
Specific Challenges for Further
Advancement
M uch progress has been made over the past several years in many
aspects o f H A B bloom ecology and dynamics. In some cases, the
linkages betw een cell physiology and toxicity have become clear.
Progress has also been made in understanding the influences o f
physical process and other environm ental param étrés integral to
harm ful algal expression. Yet, m any fundam ental physiological
processes rem ain unm easured for m ost species. N ew m ethods of
cell detection are becom ing more readily available, and progress
has been made in the identification o f some genes involved in toxin
production. F urther understanding has been gained o f the roles
o f nutrients, both inorganic and organic, in bloom development.
Similarly, the roles o f viruses and bacteria are better understood
for some H A B s. Yet, the understanding o f the interactions o f
H A B s w ith grazers, the sublethal effects o f H A B s on com m unity
dynamics, and the application o f these data in developing
predictive models is only ju st beginning.
A ccurate and tim ely identification o f harm ful species is of
fundam ental im portance to all aspects o f H A B research and
m anagem ent. H istorically, species have been delineated on the
basis o f m orphological, u ltrastructure, and life-stage features
visible in the light and electron microscopes, as well as by pigm ent
content. Increasingly, organisms are being com pared and identified
on the basis o f molecular markers such as cell surface proteins,
lipids, D N A sequences, and toxins. These same markers are serving
as a basis for rapid assays designed to detect and quantify species
specifically. W ith this progress has come an increasing dem and
for identifying organisms using traditional techniques so th a t
comparative studies and new findings regarding species diversity,
biogeography, and toxicology can be placed in an appropriate
historical context.
46
Significant advances in cellular physiology o f harm ful microalgae
have been made in the past decade w ith regard to nutrient
regulation o f toxin synthesis and assim ilation o f dissolved organic
nutrients. However, critical inform ation required for model
developm ent - such as photosynthesis-irradiance relationships,
rates o f nutrient uptake, and excretion o f organic m atter - is not
available for m ost species. Studies o f grow th rates as a function
o f tem perature, irradiance, nutrients, and th eir ratios, are rare.
M o st harm ful species employ sw im m ing or buoyancy-regulation
strategies influenced by irradiance and nutrients, in addition to
am bient tem perature and salinity, and these factors influence
population grow th and com m unity structure in ways th a t we do
not yet fully understand. The grow th rate o f many H A B s in nature
largely rem ains unknow n. Collectively, our lack o f fundam ental
knowledge concerning the basic physiology and behaviour o f most
H A B species im pedes our ability to develop predictive models th at
w ill ultim ately aid many aspects o f basic research and m anagement.
N atural resource managers and public health officials need better
tools to forecast im m inent H A B events so th a t m anagem ent
strategies can be im plem ented effectively. Forecasting capabilities
can be enhanced by im proving and expanding rem ote-sensing
technologies, such as offshore in strum ent m oorings and satellite
sensing, and th is inform ation w ill perm it m onitoring o f the
environm ental conditions th a t could lead to H A B form ation
and decline and for the tracking o f H A B s as they transit
thro u g h a region. Tim e-series analyses o f existing databases for
phytoplankton com m unities and environm ental variables such
as m acro- or m icro-nutrients, where available, are required.
Retrospective analyses o f historical data and inform ation may
provide im portant insights. In some cases, the sediments may hold
im portant historical inform ation. L and-use data, such as may be
available from maps and geographic inform ation systems may yield
trends in nutrient loadings to the landscape. W here such data are
lacking, long-term consistent m onitoring program m es m ust be
initiated in key regions where hum an influences are either know n
or are anticipated to increase. M oored instrum entation packages
- including nutrient, plankton, and optical sensors - are needed
Key Q u e stio n s
to resolve the tem poral relationships betw een nutrient inputs and
shifts in plankton composition. Shipboard observations and field
program m es would be helpful in resolving spatial differences and
in the collection o f samples for w hich sensors are not currently
available.
The vast complexity o f th e interactions betw een H A B s and their
environm ent dictates th a t we th in k in term s o f integrative models
to address the problem in a way th a t our m ental com puting
capability cannot (Noble 2002). M echanistic ecosystem models are
widely used in marine research. M odels should be constructed at
an appropriate level o f complexity to address the hypothesis being
tested and th e data available to support it. However, in reality,
we often lack the appropriate data to support such developments.
A dditionally, we should bear in m ind th a t a w ell-constructed
m odel th a t fails can be more informative th a n one th a t succeeds.
A good model should be descriptive (represent the available data),
integrative (dem onstrate how elements interact), and explanatory
(provide biological insight). C onceptual models o f biological
systems are comm on. They are com m only used as m anagem ent
tools for predicting eutrophication (e.g., M oll and Radach
2003, T ett et al. 2003), to understand ecosystem processes (e.g.,
ecosystem dynam ics, A llen et al. 2004; response to climate change,
Taylor et al. 2002) and to predict biotic responses (e.g., Besiktepe
et al. 2003). C onceptual models can be viewed as having tw o
com plim entary roles. The first is a heuristic role, whereby they are
used to corroborate a hypothesis, illum inate areas o f fu rther study,
and identify where further empirical data are required. The second
role is as predictive tools, whereby the models are used to aid
m arine resource m anagem ent and to assess the im pact o f hum ans
on the m arine ecosystem.
T h e d a r k a r e a s n e a r t h e s h o r e l in e s h o w a r e d t id e b lo o m . K a r e n ia
BREVIS, ALONG THE S W COASTLINE OF FLO R ID A , M A R C H 2 0 0 2 . P H O T O :
J . D e s c lo itr e s , M O D I S L R R T , N A S A G S F C .
The establishm ent o f a robust m odelling approach for sim ulating
H A B dynamics in eutrophic environm ents requires the following
future work:
•
th e definition o f functional groups to describe H A B s and
fu rth er developm ent and refinem ent o f conceptual process
models; crucial to th is process is the definition o f life histories
and hence, stage-structured models; equally critical is
knowledge o f th e interaction betw een H A B s and non-H A B s
(with w hich they compete for com m on nutrients) and their
predators;
•
bioinform atics to acquire, archive, and interpret data;
•
th e construction, param etrisation, validation, and evaluation
o f appropriate m athem atical and num erical models;
•
integration o f H A B models into generic coupled
hydrodynam ic ecosystem models for comparative studies; and
•
data assimilation to improve model param étrés and forecasts,
and to quantify model errors.
W h ile the ultim ate goal is to develop whole ecosystem models,
m uch is to be gained by construction and testing o f models as an
aid to our understanding o f the biological processes underpinning
H A B form ation and demise. The basis for many biological models
has failed to keep pace w ith our understanding o f plankton biology
(Flynn 2005). The u n dertaking o f experim ents to investigate these
interactions should not be trivialised; neither should funding
bodies dismiss such needs because they “have been done before”.
Integrated studies o f experim ental research and m odelling are
few and far betw een, and few data sets from previously conducted
experim ental studies are adequate for the task.
47
5. Moving Forward in the Study of HABs
in Eutrophic Systems
/
n accordance with the GEOHAB strategy,
the approach of the Core Research Project
on HABs in Eutrophic Systems will be
comparative from the cellular to the ecosystem level.
Research that is interdisciplinary - focussing on
biological, chemical, and physical processes - will be
fostered. Research will be multifaceted as the problems
relating to eutrophication are complex, and interactions
and processes occur on a broad range of scales. Finally,
research will be international in scope to encompass the
global issues of HAB events and to benefit from the
skill and expertise gained by HAB investigators world­
A CYANOBACTERIAL (BLUE-GREEN ALGAE) BLOOM ON THE SHALLOW LAKE,
L a k e T a i h u , J ia n g s u P r o v in c e , C h i n a . P h o t o : W . W
w w w .a slo .org/ ph o to po st/
wide.
ur tsba u g h ,
.
A lthough G E O H A B is prim arily built upon a coalescence of
projects at many levels, th e Core Research Project w ill also
seek, thro u g h national funding mechanism s, to conduct a series
o f experim ents and observations th a t directly address the key
questions outlined in C hapter 4. W here possible, these efforts will
capitalize on existing platform s, program m es, or ongoing studies.
Research on th e major priority areas identified herein is welcome
w ithin the G E O H A B framework. The understanding o f this
im portant issue, and ultim ately th e m anagem ent o f nutrient loads
and im proved prediction and m anagem ent o f H A B s w ill require
the global com m unity o f scientists.
Applying the GEOHAB Approach
W
h o l e lak e a n d e x p e r im e n t a l
MESOCOSM STUDIES HAVE BEEN
USEFUL IN UNDERSTANDING THE
IMPACTS OF NUTRIENTS ON BOTH
PHYSIOLOGICAL AND ECOSYSTEM
levels.
48
P h o t o : D . S c h in d l e r .
G lobal population is rapidly increasing and concurrent changes
in land use and coastal nutrient loading have been well
established for many regions o f the world. Critical to our long­
term understanding is th e need for continuous m onitoring and
observation, to docum ent changes as they are occurring, and to
understand the processes o f change. There is a need for a global
The GEOHAB Core Research Project on HABs
in Eutrophic Systems will seek to implement
a range of comparative and interdisciplinary
approaches.
Summary of Key Research Considerations
Long-term monitoring, beyond a decade, may be
required to observe trends in population, climate, and
nutrient loading.
Research must be integrated w ith new understanding
in agricultural practices, aquacultural practices,
atmospheric emissions and deposition, and human
demography.
Ecosystem characteristics such as hydrography,
residence time, stratification, and trophic interactions
w ill impact the expression of eutrophication and HABs.
Multiple observational, experimental, and modelling
approaches w ill be required to advance the study of
HABs in relation to eutrophication.
M
e s o c o s m s t u d ie s h a v e p r o v e n t o be a n e f fec tiv e t o o l in
UNDERSTANDING POPULATION AND COMMUNITY RESPONSES TO NUTRIENT
p e r t u r b a t io n s .
R ig h t : M
Left: M
e s o c o s m s t u d ie s in
e s o c o s m s t u d ie s in
C h in a . P
hoto:
J . Ll.
L o n g Is l a n d , N Y , U S A . P h o t o : T .
Kana.
netw ork o f sites th a t are deem ed sensitive to nutrient alteration
and eutrophication. In the U nited States, numerous sites now have
more th an a decade o f data on w hich to build an understanding of
the relationships am ong population change, climate change, and
trends in nutrient quantity and composition. In E urope, numerous
sites have been designated for continuous m onitoring for benthic
biodiversity and long-term phytoplankton records are know n for
the Scandinavian, N orw egian, British, Irish, French, Iberian, and
A driatic coasts. Japan has a long history o f harm ful algal records
while C hina is rapidly expanding its coastal m onitoring and H A B specific activities. The value o f long-term records is fundam ental
in understanding relationships betw een anthropogenic change,
climate change, and H A B s. In a m anner analogous to the
establishm ent o f oceanic long-term sites such as the JG O F S
H O T (H aw aii O cean Tim e-series) and B A TS (Berm uda A tlantic
T im e Series Study) sites, long-term sites for m easuring nutrient
loading and H A B s m ust be m aintained. R ecognising the value of
these long-term records is the first step in bringing comparative
observational and m odelling approaches together.
N atural experim ents are being undertaken on a broad scale th a t
w ill im pact the expression o f eutrophication in several parts of
the world and may be deserving o f special research attention. For
example, Florida Bay, U SA , receives freshwater flow from the
Everglades, but currently this flow results from m anaged discharge
rather th a n from natural hydrological conditions (R udnick et al.
1991). Fong-term m anagem ent plans for the southern Florida
area call for restoration o f the natural flow conditions w ith in the
Everglades. Thus, key questions o f concern to both scientists and
managers are to w hat extent do nutrients originating from the
Everglades contribute to eutrophication and H A B s in Florida Bay
and how w ill they change w ith altered flow conditions? Similarly,
major engineering projects are being undertaken to alter the flow
o f the Yangtze River in C hina, where diversion o f water will
cause major changes in nutrient loading to receiving waters. These
regions are o f key interest because the existing conditions are well
characterised and thus, the im pacts o f hydrological diversion can
be quantified.
The value o f integrated experim ental studies also m ust be
underscored. Such approaches have led to enorm ous advances in
our understanding o f nutrient lim itation. For example, whole-lake
m anipulations yielded trem endous insights into the differential
regulation o f N and P lim itation in freshwater systems. M uch
was learned regarding the regulation o f prim ary production by
iron in th e IronE x and SoFex experim ents (de Baar et al. 2005), in
w hich large patches o f th e ocean were fertilised w ith iron and the
responses o f the plankton com m unity observed over days to weeks.
Such approaches are beneficial in understanding H A B responses,
both on a physiological level and also on a whole ecosystem level.
Farge-system perturbations, include nutrient additions in organic
form , may provide th e key to understanding how systems may
respond as land use and nutrient loadings are altered.
To elevate research on H A B s and eutrophication to a level
consistent w ith th e G E O H A B approach o f comparative,
international, m ultifaceted, and interdisciplinary studies, the
Core Research Project on H A B s in E u trop h ic S ystem s will
aim to undertake one or more large-scale experim ental studies
th a t w ill provide opportunities for researchers from around
th e world to participate. Such studies w ill be developed w ith
considerable discussion w ith in the broader comm unity. These
experim ental studies w ill augm ent smaller-scale studies th a t will
be linked thro u g h data sharing and smaller-scale comparative
studies. Thus, the G E O H A B Core Research Project on H A B s in
E u tro p h ic S ystem s w ill seek to im plem ent a range o f approaches.
The key questions identified in C hapter 4 w ill require different
experim ental, observational, and m odelling methodologies.
49
M oving F o rw ard
T he
p a s t s e v e r a l d e c a d e s h a v e w it n e s s e d l a r g e c h a n g e s in
TERRESTRIAL AND AQUATIC NITROGEN AND PHOSPHORUS, PRIMARILY DUE TO
HUMAN ACTIVITIES SUCH AS INTENSIVE AGRICULTURE. PHOTO: J . H a WKEY.
Co-ordination of Activities
A n im portant aspect o f international activities like G E O H A B is
the sharing o f scarce resources am ong participating nations. Such
sharing makes possible research activities o f a scale and breadth
th a t are not otherwise feasible, and therefore enable the comparison
o f ecosystems o f a sim ilar (or contrasting) type in different parts
o f the world. The C R P for H A B s in E u trop h ic S ystem s w ill
prom ote the application o f additional resources - in term s o f
scientific expertise, sam pling platform s, and equipm ent - to the
key research questions identified in this docum ent. G E O H A B
has already initiated the sharing o f expertise and developm ent o f
an international research com m unity on th e topic o f H A B s and
E u trop h ic S ystem s by supporting the Open Science M eeting in
2005.
G E O H A B Core Research Projects (CRPs) w ill be co-ordinated
by the G E O H A B Scientific Steering C om m ittee (SSC) through
the establishm ent o f separate sub-com m ittees for each C R P
composed o f SSC members and leaders o f the C R P activities.
The sub-com m ittees w ill prim arily work by correspondence, but
may meet on an opportunistic basis and when identified resources
allow for m eetings to address major planning and co-ordination
issues. The sub-com m ittees w ill w ork w ith the G E O H A B SSC
and International Program m e Office to encourage scientific
networking.
G E O H A B w ill identify, and draw the attention o f responsible
bodies to, opportunities for co-ordination o f resources th a t w ill add
value to ongoing and planned research. Individuals involved in
studying the key questions outlined herein w ill be responsible for
developing plans relating to the sharing o f expertise and equipm ent
and how they w ill contribute to th e continued co-ordination o f the
Core Research.
50
G E O H A B and the C R P sub-com m ittee w ill encourage the
publication o f results from Core Research in relevant peer-reviewed
scientific journals, w ith appropriate reference to the relationship o f
the research to m anagem ent issues as well as th e G E O H A B goals.
G E O H A B w ill also seek to aid researchers in the dissem ination
o f research results and program m e status more broadly to the
world-wide com m unity o f managers and scientists interested in
H A B s through publication o f articles in H arm ful Algae News,
the G E O H A B W eb site, and other opportunities as become
available. Each C R P sub-com m ittee w ill also be responsible for
dissem inating announcem ents o f m eetings, symposia, or other
special events, and is encouraged to form appropriate linkages and
com m unications w ith the research and m anagem ent com m unities
o f the im pacted/studied areas.
Data Management and Data Sharing
The collective value o f data is greater th a n its dispersed value,
and comparative research requires effective data sharing among
scientists w orking in different regions; therefore, data m anagem ent
and data exchange are im portant com ponents o f G E O H A B C RPs.
The developm ent o f an appropriate data m anagem ent plan is a
fundam ental and critical activity upon w hich the ultim ate success
o f G E O H A B w ill depend, and the G E O H A B SSC is working
w ith other related international marine research projects to develop
basic guidelines for data m anagem ent and sharing (see w ww .jhu.
edu/scor/D ataM gm t.htm ). Each C R P w ill need to develop its
own specific plans, conform ing w ith th e principles adopted by
GEOHA B.
G E O H A B w ill use a decentralized data m anagem ent and
distribution system w ith a centralized m etadata index, as the
program m e develops. Each C R P w ill create an inventory o f data
and data products. Each G E O H A B C R P w ill address th e long­
term archival o f observational data and data products to ensure a
lasting contribution to marine science.
M oving F orw ard
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Protocols and Quality Control
T h e I n t e r n a t i o n a l N it r o g e n I n it ia t iv e is i n t e r e s t e d in
The C R P on H A B s in E u trop h ic S ystem s w ill require
m easurem ent o f a broad suite o f param étrés th a t may differ
depending on the key question being addressed. W h ere possible,
w ell-defined, internationally agreed m ethods w ill be adopted.
Regardless, to ensure quality control, the protocols used for data
collections w ill be fully docum ented in inform ation files (metadata)
accom panying data sets. W h ere necessary, the G E O H A B SSC
w ill initiate Fram ew ork A ctivities th a t lead to developm ent o f
protocols or m ethods, or th eir intercalibration, to ensure th at
comparisons across systems can be accomplished.
THE USES OF ANTHROPOG ENIC NITROGEN (W W W .IN IT R 0G E N .O R G ) . SOURCE:
UNDERSTANDING A LL ASPECTS OF THE IMPACTS OF G LOBAL INCREASES IN
Capacity Building
G E O H A B encourages a “train in g through research” approach
th a t offers opportunities for student participation and instruction
in marine research relevant to H A B s. Exchange o f post-doctoral
fellows and senior scientists are equally im p o rtan t for the C RPs.
T raining activities th a t w ould benefit G E O H A B research will
be organised by the G E O H A B SSC and proposals for specific
train in g activities can be subm itted for endorsem ent as G E O H A B
activities.
G allo w ay et al 2 0 0 3 .
Interaction with Other International
Programmes and Projects
G E O H A B exists in the context o f several large international
program m es and projects th a t study aspects o f global change and
eutrophication th a t could be relevant to th e C R P on H A B s in
E u tro p h ic System s. Some examples include:
•
The L and-O cean Interactions in the C oastal Z one (L O IC Z )
project has compiled inform ation about the supply o f m acro­
nutrients from the land to the ocean, inform ation th a t could
be useful in studying the relationships betw een nutrient
supply, type, and ratios and H A B s.
•
The International N itrogen Initiative (IN I), under the
auspices o f the Scientific C om m ittee on Problems o f the
E nvironm ent (S C O P E ) and the International G eosphereBiosphere Program m e (IG B P), is a global effort to optim ize
nitrogen’s beneficial role in sustainable food production and
to m inim ize nitrogen’s negative effects on hum an health
and th e environm ent. A s p a rt o f its objectives, knowledge
o f the flows o f nitrogen and the related problems in several
targeted regions o f the globe are being developed w ith a goal
o f m inim izing the negative effects o f hum an health and the
environm ent. This inform ation is relevant in characterising
and defining nitrogen-based eutrophication.
•
The Integrated M arine B iogeochem istry and Ecosystem
Research (IM B E R ) project is being developed w ith a goal
o f providing a comprehensive understanding of, and accurate
predictive capacity for, ocean biological and chemical
responses to accelerating global change and the consequent
effects on th e E a rth System and hum an society. P lanned
observation and process studies related to the effects o f
nutrient inputs to coastal areas are relevant to H A B s.
Modelling Activities
As described more fully in C hapter 3 o f th is report, the G E O H A B
C R P on H A B s in E u trop h ic S ystem s w ill require application
o f a range o f m odelling approaches. The C R P on H A B s in
E u tro p h ic S ystem s should interact w ith the G E O H A B M odelling
Subcom m ittee to compare models, to participate in model inter­
com parison exercises, and share approaches. M odelling w ithin
H A B s in E u trop h ic S ystem s m ust also recognise the im portance
o f global nutrient, clim ate, and population models in additional to
models o f population dynamics o f H A B s per se.
51
Moving F o rw ard
Hunan
Sysiwn
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i L
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MARINE
B f o g e o c ^ ie a '
C ydes
T h e I M B E R p r o j e c t is d e s ig n e d t o s t u d y t h e im p a c t s o f
ANTHROPOG ENIC A N D CLIM ATIC CHANGE EFFECTS O N BIOGEOCHEM ICAL
PROCESSES IN THE OCEAN ( I M B E R 2 0 0 5 ) .
The C lim ate Variability and Prediction (C LIV A R ) project is
studying how climate oscillations, such as E N S O and N A O ,
operate and are expressed in the ocean and atmosphere.
Interactions betw een climate change and eutrophication are
identified as one o f the key questions o f interest to H A B s in
E u trop h ic System s.
In summary, with the aid of co-ordination facilitated
by the CRP committee and the GEOHAB SSC as
a whole, the activities of core research of HABs in
Eutrophic Systems will strive to undertake studies
that directly address the key questions identified and
The G lobal O cean O bserving System (G O O S ) is a
program m e for sustained, co-ordinated international
observations o f the ocean and a platform for th e generation
o f oceanographic products and services. H A B s in E u trop h ic
S ystem s recognises th a t traditional approaches for detecting
nutrient concentrations are often inadequate to resolve
short-term pulses o f nutrient loading th a t may precede H A B
outbreaks. As new technologies in nutrient m onitoring and
cell detection move into operational status, the interactions
betw een G O O S and H A B s in E u tro p h ic S ystem s will
become strengthened.
The G lobal O cean Ecosystem D ynam ics (G L O B E C ) project
is focussed on understanding the relationship betw een
physical processes and Zooplankton in the support o f
marine fisheries. A ctivities o f this project w ill be o f direct
relevance to H A B s in E u trop h ic S ystem s in determ ining the
interactions “top dow n” and “bottom up” factors in controlling
H A B s.
52
to become integrated with many projects at many
levels, in order to advance and communicate scientific
understanding of the role of eutrophication in the
global proliferation of HABs. GEOHAB invites all
relevant contributions to this effort.
WRÈOF
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F is h a n d W il d l if e , N e w J e r s e y F ie l d O f f ic e ; P. G l ib e r t ; C a n a d a D e p t , o f F is h e r ie s a n d O c e a n ; a n d K . W h i t i n g - G r a n t , M a i n e S e a G r a n t .
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65
A p p e n d i x I:
GEOHAB
O p e n S c ie n c e M e e t in g o n
H AB s a n d
E u tr o p h ic a tio n , M a r c h 2 0 0 5
Programme
M on d ay, M arch 7, 200S
SE S SIO N 1
T R E N D S IN E U T R O P H IC A T IO N A N D H A B S
12:00-13:30
(Session C hair: Patricia M . G libert)
O pening Remarks - Patricia M . G libert (USA)
N itrogen pollution: sources, trends, and effects globally and regionally - R obert H o w arth (USA)
C O FFE E BREAK
N ational and global trends in H A B s - D onald A nderson (USA)
M ultidecadal changes in the diatom: Flagellate ratio and Si:N and Si:P ratios in N arragansett Bay, and influence o f SI
N supply ratios on diatom species com petition - Ted Smayda (USA) and D. B orkm an
LUNCH
SE S SIO N 2
P H Y S IO L O G Y A N D E C O L O G Y O F H A B S W I T H R E S P E C T T O N U T R I E N T S
9:15- 9:45
9:45 - 10:25
10:25-11:00
11:00-11:30
11:30-12:00
13:30-14:10
14:10-14:30
14:30-14:50
14:50-15:15
15:15- 15:35
15:35- 15:55
15:55- 16:15
16:15 -16:45
16:45- 17:05
17:05-17:30
17:30- 19:30
(Session Chairs: E dn a G ranéli and C indy H eil)
The role o f nutrient conditions on toxicity, allelopathy, and m ixotrophy in H A B s - E d n a G ranéli (Sweden)
N itrogen uptake by the toxigenic diatom Pseudo-nitzschia australis - W illiam C ochlan (USA), J. H erndon, N .C .
Ladizinsky and R .M . Kudela.
U rea-am m onium -nitrate interactions in Thau lagoon (Southern France): Relationships w ith Alexandrium catenella
blooms - Yves Collos (France), A . Vaquer, M . Laabir, E. A badie, T. Laugier, and A . Pastoureaud
BREAK
A role for anthropogenically derived nitrogen in the form ation o f harm ful algal blooms along th e US w est coast
- Raphael Kudela (USA), M . A rm strong, W. C ochlan, and J. H erndon
N itrogen preference o f the fish-killing flagellate Chattonella cf. verruculosa - Carm elo Tomas (USA)
Intraspecific variability in the nutritional ecology o f harm ful algae - Jo A n n Burkholder (USA)
The effects o f macro- and m icro-nutrient lim itation on karlotoxin production by Karlodinium micrum strains - Jason
A d o lf (USA), T. Bachvaroff, G.F. Reidel, and A . R. Place
Effect o f N :P supply ratio on biochem ical com position and toxicity in dinoflagellate Alexandrium tamarense - A i M urata
(Japan), S. C. Y. Leong, Y. N agashim a, and S. T aguchi
O pen discussion
Poster Session O ne (see page 68)
(H osted by th e U niversity o f M aryland C enter for E nvironm ental Science, the Chesapeake Research C onsortium , and
the M aryland D ep artm en t o f N atural Resources)
T uesday, M a rch 8 , 2005
SE S SIO N 3
T H E G E O H A B P R O G R A M M E A N D O T H E R IN IT IA T IV E S
8:30-8:45
8:45-9:05
9:05-9:35
9:35-9:55
9:55-10:20
SE S SIO N 4
1 0 : 2 0 - 11:00
11:00-11:40
11:40-12:20
12:20-14:00
14:00-14:40
14:40-15:00
66
(Session C hair: D onald A nderson)
Introduction to the G E O H A B Program m e - G ran t Pitcher (S. Africa)
Introduction to IO C and S C O R - H en rik Enevoldsen (IO C ) and E d U rban (SC O R)
N O A A extram ural H A B research: Present and future - Q uay D ortch (USA), S. B anahan, and M . Suddleson
Perspectives o f the US O cean Com m ission and the Pew O ceans Com m ission - D onald Boesch (USA)
C O FFE E BREAK
C O M P A R A T IV E S T U D I E S A N D IN T E R N A T IO N A L P R O G R A M M E S O N H A B S IN E U T R O P H IC
AREAS
(Session Chairs: M ingjiang Z hou and Lars Edler)
The C hinese H A B Program m e: C E O H A B - M ingjiang Z hou (China)
D o the coastal eutrophication and w arm ing cause w idespread and persistent Cochlodiniumpolykroides blooms in Korean
waters? - H akG yoon Kim (Korea), C -K . Lee, W -A . Lim , S-Y. K im , and H -G . Jin
Influence o f monsoons and oceanographic processes on red tides in H o n g Kong waters - Kedong Yin (H ong Kong
China)
LUNCH
H arm fu l algae and eutrophication in the Baltic Sea A rea - L ars E dler (Sweden)
O ceanographic and environm ental assessment o f K uwait’s waters in relevance to algal blooms - Faiza Al-Yamani
(Kuwait), W .A . Ism ail, K.S. A l-R ifaie, and A . Lennox
15:00-15:20
15:20-15:45
15:45-16:05
16:05-16:25
16:25-16:45
16:45-17:30
H A B s in W estern A ustralia: Expressions o f eutrophication in a southern climate - M alcolm Robb (A ustralia), T.
Reitsem a, W . Hosja, and A . Begum
BREAK
A n integrated approach to predicting harm ful algal blooms: Phytoplankton physiology, nutrient dynamics and their
application in an ecosystem model - Paul A rm strong (A ustralia), P A . Thom pson, C.J.S. Bolch, S.I. B lackburn, J.P.
Parslow, M . H erzfeld and K. W ild-A lien
C om parative analysis o f the relationships betw een nutrient cycling and phytoplankton com m unity com position in tw o
eutrophied subtropical estuaries: Florida Bay, U SA , and M oreton Bay, A ustralia - C ynthia H eil (USA), P.M . G libert,
J. O ’N eil, W .C . D ennison, D. H ollander, J. G reenw ood, M . O ’D onohue, S. C ostanzo, M . Revilla, J. Alexander, A.
H oare, and S. M urasko
Linkages betw een land-based nutrient discharges and harm ful m acroalgal blooms: C om parative studies on coral reefs
o f southeast Florida and Jam aica - Brian Lapointe (USA), B. B edford, P.J. Barile, C. H anson, and L. G etten
O pen discussion
W ed n esd ay, M a rch 9 , 2005
S E S SIO N 5
M A C R O N U T R IE N T IN T E R A C T IO N S W IT H O T H E R F A C T O R S C O N T R O L L IN G H A B S
8:30-8:50
8:50-9:10
9:10-9:30
9:30- 9:50
9:50- 10:20
10:20-10:40
10:40-11:00
11:00- 11:20
S E S SIO N 6
(Session C hair: Ted Smayda)
H o w does eutrophication affect th e role o f grazers in harm ful algal bloom dynamics? - E dw ard Buskey (USA)
Freshwater flow and nutrients: effects on top-dow n control o f bloom -form ing dinoflagellates? - D iane Stoecker (USA),
M .L . Reaugh, A .E . Thessen, D .E . G ustafson, M .R . R om an, and W .C . Boicourt
A conceptual model for ecosystem disruptive algal blooms: The interactive roles o f eutrophication, algal toxicity, and
lim itation by nutrients and lig h t - W illiam Sunda (USA) and R. H ardison
Abiotic and biotic factors controlling a nutrient driven dinoflagellate bloom and likely responses to increased
eutrophication - R. W ayne L itaker (USA) and P A . Tester
C O FFE E BREAK
Brackish storm w ater detention ponds as prom oters o f H A B s and eutrophication along the South C arolina coast - A lan
L ew itus (USA), M .K . Burke, L. J. M ason, K. N . Bunker, S.R. D rescher, and W .H .J. Strosnider
Iron induced developm ent pathw ay o f H A B s com m unity and its consequence on m itigation o f eutrophication - Jun Sun
(China), Y. Feng, and P. Sun.
The synergy o f iron, copper and the toxicity o f diatom s - M a rk W ells (USA), C. G . T rick, W .P. C ochlan, P. H ughes,
and N . C. Ladizinsky
N E W C H A L L E N G E S A N D M E T H O D O L O G IE S
11:50-12:30
12:30-14:00
(Session C hair: M are Suddleson)
Im plem enting the coastal module o f the Global O cean O bserving System (G O O S ): Toward rapid detection and tim ely
predictions o f harm ful algal blooms - Thomas M alone (USA)
N ew approaches and technologies for observing harm ful algal blooms - M arcel Babin (France)
LUNCH
SE S S IO N 6
(con tin u ed )
11:20-11:50
14:00-14:20
14:20-14:40
14:40-15:00
15:00-15:30
15:30-15:50
15:50-16:10
16:10-16:40
16:45-18:45
(Session C hair: M arcel Babin)
A pplication o f the environm ental sample processor (ESP) for rem ote detection o f harm ful algae and toxins they produce
- C hris Scholin and G reg D oucette (USA)
A utonom ous nutrient m onitoring and water sam pling as tools for studying H A B s: Progress and prospects- L ou
C odispoti (USA), V. Kelly, P. G libert, and J. A lexander
N ew technologies for m onitoring and assessing harm ful algal blooms and water quality in Chesapeake Bay, M aryland
- C hristopher H eyer (USA), T. M .Trice, P. J. T ango, B .M ichael, L .C odispoti, V. Kelly
BREAK
D iagnostic indicators o f H A B nutritional physiology - Sonia D yhrm an (USA)
N ew approaches to understanding the role o f dissolved organic m atter in H A B dynamics - Sybil Seitzinger (USA), P.
M . G libert, J.P. Simjouw, and R. Sipler
O pen discussion
Poster Session Two (see page 69)
67
Program m e
Thursday, M a rch 10, 2 0 0 5
SE S SIO N 7
M O D E L L IN G O F N U T R IE N T S A N D H A B S
8:30- 9:10
9:10- 9:50
9:50-10:10
10:10- 10:40
10:40- 11:00
11:00-11:30
(Session Chairs: J. Icarus A llen and Kevin Flynn)
E utrophication and H A B models for the N W E uropean continental s h e lf - J . Icarus A llen (UK), F. G ilbert, J. H olt,
M . H o lt, R. Proctor, a n d j. Siddorn
G arbage in, G arbage out? Problems in experim ental design and m odelling o f H A B ecology - Kevin Flynn (Wales)
C O FFE E BREAK
Assessing the validation o f a prelim inary Karlodinium micrum nowcast model system in Chesapeake Bay and its
tributaries: a fram ew ork for H A B nowcasts and forecasts - Peter Tango (USA), C.W . Brown, T.F. Gross, D .L.
Ram ers, R .R . H ood, and B.D. M ichael
M odelling Pfiesteria life cycle attributes and population dynamics - Raleigh H o o d (USA), X . Z hang and J.T. A nderson
O pen discussion o f m odelling
SE S SIO N 8
G E O H A B IM P L E M E N T A T IO N
11:30-11:45
11:45-12:45
12:45-14:15
14:15-14:45
14:45-16:00
16:00-16:15
16:15-16:45
16:45
17:00
(Session C hair: G ran t Pitcher)
C harge to w orking groups - Patricia G libert and G ran t Pitcher
F irst break-out groups m eet
LUNCH
Reports o f first break-out groups
Second break-out groups meet
BREAK
Reports o f second break-out groups
Final w rap-up
A djourn
M on d ay, M arch 7, 2 0 0 5
P O S T E R SE S SIO N O N E
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
68
Phytoplankton indices o f eutrophication in U K coastal waters - R.J. G owen, D .K. M ills, M . Best, M .J. D evlin, M . Edw ards, J.
Foden, S.J. Painting, R. Park, C. Reid, and P. T ett
E utrophication and harm ful algal blooms in the Swan River estuary, W estern A ustralia - J. John
The research o f the eutrophication status o f E ast C hina Sea - X .- L . W ang, X.-Y. Shi, and C .-S. Z hang
C oastal nutrification following th e passage o f H urricane Charley and its relation to a subsequent Karenia brevis bloom on the W est
Florida S h e lf -M .B . Neely, C .A . H eil, and G .A . Vargo
The effect o f nutrient concentration at different grow th stages on hemolytic ability o f three clones o f the ichthyotoxic flagellate
Prymensium parvum from blooms in the U nited States - M . Clouse and C. Tomas
Strain Variation in Karlodinium micrum toxin production - T. Bachvaroff, J.E . A dolf, and A .R . Place
Fatty acids and grow th in the heterotrophic dinoflagellates Pfiesteria Spp. and P L O s - L.W . H aas, V. Foster, L. O tt, W .K . Vogelbein,
K.S. Reece, J.D . Shields, and P. M ason
The influence o f dissolved copper on the production o f domoic acid by toxigenic species o f Pseudo-nitzschia in M onterey Bay,
C alifornia - N .C . Ladizinsky, G.J. Sm ith, K .H . Coale, and W .P. C ochlan
Toxin levels in the benthic cyanobacterium Lyngbya majuscula in relation to tissue nutrient content and bloom intensity - J.M . O ’Neil,
S. A lbert, N . O sborne, and G . Shaw
The potential role o f increased nutrient inputs to higher incidences o f ciguatera in H aw aii - M .L . Parsons
N utrient regulation o f toxin production: C om parison o f hemolytic activity o f Amphidinium carterae and Amphidinium klebsii
- L .A .
Z im m erm ann and C .R . Tomas
N itrate uptake kinetics o f th e toxic dinoflagellate Alexandrium tamarense in response to nitrate supply mode - S.C.Y. L eong, M .
M aekaw a, and S. T aguchi
Bioavailability o f dissolved organic phosphorus compounds to typical harm ful dinoflagellate Prorocentrum donghaiense L u - B. H uang,
L. O u, H . H ong, H . Luo, and D. W ang
Dissolved organic m atter concentration and characteristics during Aureococcus anophagefferens blooms in 2002 and 2003: A comparison
- J.-P.Simjouw, E .C . M inor, and M .R . M ulholland
The role o f natural D O M sources in Prorocentrum minim um grow th dynamics - R. Sipler, S.P. Seitzinger, and P.M . G libert
Urea utilisation by harm ful algal species in the Chesapeake Bay, M aryland, U SA - C .M .
Solomon and P.M . G libert
A com parison o f nutrient effects on the grow th o f Chattonella subsalsa and Heterosigma akashiwo (Raphodophyceae) isolated from the
Inland Bays, Delaware (U .S.A) - Y. Z h an g and D .A . H utchins
The assessment o f brow n tide blooms caused by the alga, Aureococcus anophagefferens and related environm ental factors in coastal waters
o f N ew Jersey (2000-2002) - M . Downes G astrich, R. L athrop, S. H aag, M .P. W einstein, M . D anko, D .A . C aron, and R. Schaffner
H arm fu l algae in Suffolk C ounty (N.Y., USA) estuaries: A 30 year history - R. N uzzi
O rganic nutrients and brow n tide in M aryland C oastal Bays - C. W azniak
Program m e
W ed n esd ay, M a rch 9 , 2005
P O S T E R SE S SIO N T W O
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
Top down control and demise o f a nutrient driven dinoflagellate bloom - P.A. Tester and R.W. Litaker
M odelling the contribution o f prey deselection in th e form ation o f harm ful algal blooms - A. M itra and K.J. Flynn
Raphidophyte systematics and rapid identification: Sequence analyses and real tim e P C R Assays - H .A . Bowers, C. Tomas, J.W.
K em pton, S. G oto, A.J. L ew itus, and D.W. O ldach.
G eographic distribution o f Pfiesteria spp. and environm ental factors - H . Z hang and S. L in
Im proved accuracy o f quantitative real-tim e P C R o f H A B species in environm ental water samples using an exogenous D N A internal
standard - K.J. C oyne, S.M . H andy, E. D em ir, K.J. P ortune, Y. Z hang, M .A . D oblin, D .A . H utchins, and S.C. C ary
H arm fu l phytoplankton indicator species applied to eutrophication assessments o f Scottish coastal waters supporting aquaculture
- M .J. G ubbins, P.J. Sammes, and I.M . Davies.
M onitoring toxic phytoplankton and shellfish in support o f eutrophication assessments for Scottish coastal waters - M .J. G ubbins,
E .A. Sm ith, M . G rieve, and E. Bresnan
H istory o f H A B m onitoring in M aryland tidewaters: M onitoring, response, nowcasting and forecasting - P.J. Tango, B. M ichael, D.
G oshorn, R. M agnien, C. Heyer, T .M . Trice, W . Butler, C. W azniak, R. K arrh, S. Bowen, R. Lacouture, H . Bowers, D. O ldach, C.
L uckett, C. Poukish, D. M atuzsak, J. Ryan, H . L ynch, C. Brown, R. H ood, T. Gross, and D. Ramers
A n autonom ous urea m onitor for studying H A B s - V. Kelly, L .A . C odispoti, P. G libert, and J. A lexander
A pplications o f an in situ water quality m onitoring platform (M A R V IN ) for H A B research: A com parison o f data collected in the St.
Johns and C aloosahatchee River systems in Florida - J. Rueter, M .B . Neely, B. Bendis, R. Pigg, K. Steidinger, and C. H eil
R elationships betw een nitrogen loading and concentrations o f nitrogen and chlorophyll in coastal embayments - E .H . D ettm ann,
L .B . M ason, A . Erhunse, and K .M . H enry
M odeled Karenia brevis bloom initiation and subsequent accum ulation in the vicinity o f a coastal nutrient front - G .S. Janow itz and D.
Kamykowski
Ecosystem m odelling o f th e N W E uropean shelf seas tow ards th e forecasting o f harm ful algal blooms - J.R . Siddorn, J.I. A llen, and
M . H olt
E nvironm ental and behavioural influences on Karenia brevis’ nitrate uptake: A bloom initiation scenario - G . Sinclair, D.
Kamykowski, E. M illig an , and B.Schaeffer
A behaving drifter for sim ulating tran sp o rt o f mobile H A B organisms in nature - T .G . W olcott, D. Kamykowski, and G . Janow itz
Potential roles o f Prorocentrum minimum to Chesapeake Bay dissolved oxygen and oyster dynamics - E. Brownlee, S. Sellner, and
K .G. Sellner
Volunteer H A B m onitoring provides a “F irst W atc h ” for resource managers and researchers in th e Delaware In lan d Bays, U SA - E.
W hereat and M . Farestad
Problems w ith ballast water exchange as a means o f controlling m ovem ent o f harm ful algal species th roughout th e world - C .E .
O rano-D aw son, R. D awson, and D .A . W right
69
A p p e n d i x II:
GEOHAB
O p e n S c ie n c e M e e t in g o n
HABs a n d
E u tr o p h ic a tio n , M a r c h 2 0 0 5
Participants
Jason Adolf
Patrick Conway
Robert Gross
B a l t im o r e , M D U S A
W a s h in g t o n , D C U S A
W il m in g t o n , D E U S A
J. Icarus Allen
Kathryn Coyne
M att Gubbins
P ly m ou th U N I T E D K IN G D O M
L ew es, D E U S A
A berdeen U N I T E D K IN G D O M
Khlood Al-Rifaie
Ifeyinwa Davis
Leonard W. Haas
K u w a it K U W A IT
W a s h in g t o n , D C U S A
G l o u c e s t e r P o in t , VA U S A
Donald M. Anderson
Edward Dettmann
Callie Haii
W
N arrag a nsett, R I U S A
S t e n n is S pace C e n t e r , M S U S A
o ods
H
ole,
M A USA
Paul Armstrong
Felisa Diaz-Mendez
Matthew R. Haii
H
B a l t im o r e , M D U S A
A n n a p o l is , M D U S A
obart,
T a s m a n ia A U S T R A L IA
Marcel Babin
L. Kellie Dixon
Paul E. Hargraves
Sa r a s o t a , E L U S A
N a rrag a nsett, R I U S A
Tsvetan Bachvaroff
Quay Dortch
Cynthia Heil
B a l t im o r e , M D U S A
S ilv er S p r in g , M D U S A
St . P e t e r s b u r g , E L U S A
Susan Banahan
Gregory Doucette
Julian Herndon
S ilv er S p r in g , M D U S A
C h a r l e s t o n , SC U S A
T ib u r o n , C A U S A
V il l e f r a n c h e - su r - M
er
FRA N CE
Jennifer Berrigan
Sonya Dyhrman
Christopher Heyer
W a s h in g t o n , D C U S A
W
A n n a p o l is , M D U S A
oods
H
o le,
M A USA
Donald Boesch
Lars Edler
Raleigh R. Hood
C a m b r id g e , M D U S A
A n gelholm S W E D E N
C a m b r id g e , M D U S A
Holly Bowers
Henrik Oksfeldt Enevoldsen
Robert W. Howarth
B a l t im o r e , M D U S A
C o pen h a g en D E N M A R K
It h a c a , N Y U S A
Larry Brand
Chunlei Fan
Bangqin Huang
M
B a l t im o r e , M D U S A
X ia m e n P.R . C H I N A
JoAnn Burkholder
Muns Farestad
Edythe M. Humphries
R a l e ig h , N C U S A
L ew es, D E U S A
D over, D E U S A
ia m i,
EL USA
Edward Buskey
Betty June Farkas
Muna Hussein
P o r t A ra nsa s, T X U S A
G a it h e r s b u r g , M D U S A
A l S u r r a h K U W A IT
Melissa Clouse
Kevin John Flynn
Dave Hutchins
W il m in g t o n , N C U S A
Sw a n se a U N I T E D K I N G D O M
L ew es, D E U SA
William Cochlan
Patricia Glibert
Gerald Janowitz
T ib u r o n , C A U S A
C a m b r id g e , M D U S A
R a l e ig h , N C U S A
Lou Codispoti
David Goshorn
Andrew Juhl
C a m b r id g e , M D U S A
A n n a p o l is , M D U S A
P a l is a d e s , N Y U S A
Yves Collos
Edna Granéli
Vince Kelly
K alm ar S W E D E N
C a m b r id g e , M D U S A
M
o n t p e l l ie r
70
FRA N CE
Darla Konkel
W a sh in g to n ,
D C U SA
Robert Nuzzi
R i v e r h e a d , N Y USA
Dana Sipek
W a sh in g to n ,
D C U SA
HakGyoon Kim
R E P U B L IC O F K O R E A
Garvan O'Donnell
B usan
P a rk m o re , G a lw a y
Judy Kleindinst
W o o d s H o l e , M A U SA
Judith M. O'Neil
C a m b r i d g e , M D U SA
Ted Smayda
Raphael Kudela
S a n t a C r u z , C A U SA
A n n a p o lis,
Celia Erlinda F. Orano-Dawson
M D U SA
Caroline M. Solomon
C a m b r i d g e , M D U SA
V ero B each,
Brian E. Lapointe
EL U SA
Troy C. Osborne
W a s h i n g t o n , D C U SA
Diane Stoecker
C a m b r i d g e , M D U SA
B u ie s C r e e k ,
L. Michael Larsen
N C U SA
W a sh in g to n ,
Pia Marie Paulone
D C U SA
W ilm in g to n ,
Sandric Chee Yew Leong
JA P A N
Grant Pitcher
C a p e T o w n S O U T H A F R IC A
Mare Suddleson
S i l v e r S p r i n g , M D U SA
Alan J. Lewitus
Allen Place
Jun Sun
Tokyo
Rachel Sipler
IR E L A N D
N a rra g a n se tt,
R I U SA
Peter Strilko
D E U SA
USA
B a ltim o re ,
M D U SA
A n n a p o lis,
Rebecca Raves
M D U SA
William Sunda
B e a u f o r t , N C U SA
Senjie Lin
G r o t o n , C T U SA
Tarren Reitsema
E a s t P e r t h A U S T R A L IA
A n n a p o lis,
R. Wayne Litaker
N C U SA
Malcolm Robb
E a s t P e r t h A U S T R A L IA
Robert Magnien
S i l v e r S p r i n g , M D U SA
Jason Rueter
C h a rle s to n , SC
Ji Li
C a m b rid g e,
B eau fo rt,
S t.
M D U SA
N J U SA
N ew B ru n sw ick ,
EL U SA
P e te rsb u rg ,
Thomas C. Malone
A r l i n g t o n , VA U SA
W ilm in g to n ,
W a sh in g to n ,
Anne S. Marsh
D C U SA
N e w B ru n sw ick ,
Bruce Michael
M D U SA
Kevin Sellner
E d g e w a t e r , M D U SA
Aditee Mitra
S w a n s e a U N IT E D K IN G D O M
John Siddorn
Ai Murata
JA P A N
Jean-Paul Simjouw
A n n a p o lis,
Tokyo
P e te rsb u rg , EL
D E U SA
Sybil Seitzinger
N J U SA
U N IT E D K IN G D O M
Geoff Sinclair
USA
R a le ig h , N C
P R C H IN A
Peter Tango
M D U SA
Avery O. Tatters
C a ro lin a B each,
N C U SA
Patricia A. Tester
N C U SA
B eau fo rt,
Helge Abildhauge Thomsen
C h a r l o t t e n l u n d DENM ARK
Carmelo R. Tomas
N C U SA
W ilm in g to n ,
Charles Trick
L o n d o n CANADA
EricTurevon
E x e te r, D evon
N e w B ru n sw ick , N J
Merrie Beth Neely
S t.
Paul Sample
Q in g d a o
W a sh in g to n , D C
U SA
Ed Urban
U SA
B a ltim o re , M D
U SA
Cathy Wazniak
USA
A n n a p o lis, M D
U SA
Participants
E d w a rd W h e re a t
D E USA
Lew es,
R o b e r t W h it m a n
N ew ark,
D E USA
A m a n d a W illa r d
W a sh in g to n ,
D C USA
T h o m a s G . W o lc o tt
R a le ig h ,
N C USA
K e d o n g Y ln
G uangzhou
R R . C H IN A
YaohongZhang
Lew es,
D E U SA
M in g jia n g Z h o u
Q in g d a o
R R . C H IN A
L e ig h Z im m e r m a n n
W ilm in g to n ,
72
N C U SA
A p p e n d ix III: G lobal E cology a n d O c e a n o g r a ph y of H a r m f u l
A lgal B loom s
S c ie n tific S te e r in g C o m m itte e fo r
G EO H A B 2006
Raphael M. Kudela
USA
Members
Robin Raine
C
h a ir
, I
K U D E L A @ U C S C .E D U
reland
R O B IN .R A IN E @ N U IG A L W A Y .IE
Alicia Lavin
S pa in
Marcei Babin
V ic e -c
, F
h a ir
m arcel
@
a l i c i a .l a v i n
o b s - v l f r .f r
Dennis McGillicuddy
USA
Allan Cembella
(ex-
o ffic io
C R P ), G
, C
@ s t .i e o .e s
rance
o
D M C G IL L IC U D D Y @ W H O I.E D U
-C
h a ir of
F jo rd s
and
C
oastal
E
mbayments
erm any
Grant Pitcher
a c e m b e lla @ a w i-b re m e rh a v e n .d e
(ex -o ffic io , C h a i r o f U p w e llin g S y stem s
C R P ),
S o u th
A fric a
Einar Dahl
N ORWAY
g p itc h e r@ sfri2 .w c a p e .g o v .z a
E in a r.D a h l@ im r.n o
Beatriz Reguera
(ex -o ffic io , C h a ir ,
Wolfgang Fennel
(ex-
o ffic io
, C
h a ir of
w o l f g a n g .f e n n e l
IP H A B ),
S p a in
b e a triz .re g u e ra @ v i.ie o .e s
M
@ io -w
o d el l in g
Su
b c o m m it t e e
), G
erm any
a r n e m u e n d e .d e
Mingjiang Zhou
C
Ken Furuya
h in a
-B
m jzh o u
e ijin g
@
m s .q d i o .a c .c n
Japan
FU R U Y A @ F S. A .U -T O K Y O .A C .JP
Sponsor Representatives
Patrick Gentien
(ex-
o ffic io
pg e n t ie n
@
, C
h a ir of
St r a
t if ie d
Sy s t e m
s
C R P ), F
rance
i f r e m e r .f r
H A B @ B O T .K U .D K
Patricia Glibert
(ex -o ffic io , C h a i r o f E u tr o p h ic S y stem s
G L IB E R T @ H P L .U M C E S .E D U
Henrik Enevoldsen
IO C
C R P), USA
Ed Urban
SC O R
E
d
.U r b a n @ j h
u .e d u
Leonardo Guzmán
C
h il e
L G U Z M A N @ IF O P .C L
73
Figure Credits
p. 13. Model-predicted export of dissolved inorganic nitrogen. Reprinted from Seitzinger and Kroeze (1998), Global Distribution
o f Nitrous Oxide Production and N Inputs in Freshwater and Coastal Marine Systems. Global Biogeochemical Cycles 12:100, with
permission from Springer Science and Business Media.
p. 15. Contribution by global region. Reprinted from Glibert et al. (2005), The Role o f Eutrophication in the Global Proliferation o f
Harmful Algal Blooms. Oceanography 18(2):200, w ith permission from The Oceanography Society.
p. 17. Sewage plume map. Reprinted from Dennison and Abal (1999), Moreton Bay Study. Published by the Southeast Regional Water
Quality Management Strategy, p. 131 w ith permission from the authors.
p. 17. Increasing HAB occurrence. Reprinted from Granéli (2005), Eutrophication and harmful algal blooms, Chapter 7 in P. Wassmann,
and K. Olli (eds.), Drainage Basin Inputs and Eutrophication, w w w .ut.ee/~olli/eutr/, w ith permission from the author.
p. 17. The relationship between population growth. Redrawn from Trainer et al. (2003), Paralytic Shellfish Toxins in Puget Sound,
Washington. Journal o f Shellfish Research 22:221, w ith permission from the journal.
p. 18. The change in N:P ratio. From Anderson et al. (2002), based on Riegman (1995), Harmful Algal Blooms and Eutrophication:
Nutrient Sources, Composition and Consequences. EstuarieslS (4b):714, w ith permission from the Estuarine Research Federation.
p. 19. The relationship between the percent contribution of urea to total N uptake. Reprinted from Glibert and Heil (2005). Use
o f Urea Fertilizers and the Implications for Increasing Harmful Algal Blooms in the Coastal Zone. Contributed papers, the 3rd
International Nitrogen Conference, Science Press USA Inc., 2005, p. 542, w ith permission from the authors.
p. 20. Prorocentrum minimum blooms in the tributaries of Chesapeake Bay. Reprinted from Fan et al. (2003), Characterization o f
the A ffin ity for Nitrogen, Uptake Kinetics, and Environmental Relationships for Prorocentrum minimum in Natural Blooms and
Laboratory Cultures. Harmful Algae 2:293, w ith permission from Elsevier.
p. 34. Marine pelagial habitats. From Smayda and Reynolds (2002), Community Assembly in Marine Phytoplankton: Application o f
Recent Models to Harmful Dinoflagellate Blooms. Journal o f Plankton Research 23:456, with permission from Oxford University Press.
p. 36. Physical environments interact w ith organism behaviour. From McGillicuddy et al. (2003), A Mechanism for Offshore Initiation
o f Harmful Algal Blooms in the Coastal Gulf o f Maine. Journal o f Plankton Research 25(9):1131 -1138, w ith permission from Oxford
University Press.
p. 38. Conceptual relationships. Redrawn from MacIntyre et al. (2005), Mediation o f Benthic-Pelagic Coupling by Microphytobenthos:
and Energy- and Material-Based Model for the Initiation o f Blooms o f Aureococcus anophagefferens. Harmful Algae 3:421, with
permission from Elsevier.
p. 42. Change in US atmospheric NOx emissions. Reprinted from Howarth et al. (2002b), Nitrogen Use in the United States from 19612000 and Potential Future Trends. Ambio 31 (2):89, w ith permission from The Royal Swedish Academy of Sciences.
p. 42. The relationship between human inputs of N and riverine N export. Reprinted from Howarth et al. (1996), Regional nitrogen
budgets and riverine N and P fluxes. Biogeochemistry35 (1):75-139, w ith permission from Springer Science and Business Media.
p. 44. Short-term nutrient loading, such as occurred following Hurricane Isabel. Reprinted from Miller et al. (2006), Hurricane Isabel
Generated an Unusual Fall Bloom in Chesapeake Bay. Geophysical Research Letters 33, L06612, w ith permission from the American
Geophysical Union.
p. 45. Possible long-term relationship. Reprinted from Alvarez-Salgado et al. (2003), The Portugal Coastal Counter Current O ff NW
Spain: New Insights on Its Biochemical Variability. Progress in Oceanography 56:281-321, with permission from Elsevier.
p. 51. The International Nitrogen Initiative. Reprinted from Galloway et al. (2003), Emerging Challenges- New Findings. The Nitrogen
Cascade: Impacts o f Food and Energy Production, Overfishing: Harvesting Fish Faster Than They Can Reproduce. GEO Year Book
2003, p. 57, w ith permission from the author.
74
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