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Harmful Algae. Author manuscript; available in PMC 2017 August 04.
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Published in final edited form as:

Harmful Algae. 2008 December ; 8(1): 3–13. doi:10.1016/j.hal.2008.08.006.

Eutrophication and Harmful Algal Blooms: A Scientific

Consensus
J. Heisler1,*, P. Glibert2,#, J. Burkholder3, D. Anderson4, W. Cochlan5, W. Dennison2, C.
Gobler6a,6b, Q. Dortch7, C. Heil8a,8b, E. Humphries9, A. Lewitus10a,10b, R. Magnien11a,11b, H.
Marshall12, K. Sellner13, D. Stockwell14, D. Stoecker2, and M. Suddleson7
1U.S.EPA, Oceans and Coastal Protection Division, Marine Pollution Control Branch, 1200
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Pennsylvania Avenue, N.W., Washington, DC 20460

2University
of Maryland Center for Environmental Science, Horn Point Laboratory, PO Box 775,
Cambridge MD 21613
3Center for Applied Aquatic Ecology, North Carolina State University, Raleigh, NC 27695
4Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543
5Romberg Tiburon Center for Environmental Studies, San Francisco State University, Tiburon, CA
94920
6aDepartment of Biology, Southampton College – Long Island University, Southampton, NY 11968
7National Oceanic and Atmospheric Administration, 1305 East West Highway, Silver Spring, MD
20910
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8aCollege of Marine Science, University of South Florida, St. Petersburg, FL 33701

9DelawareDepartment of Natural Resources and Environmental Control – Division of Water
Resources, Dover, DE 19901
10aBelle W. Baruch Institute of Marine Science and Coastal Research, and University of South
Carolina, Baruch Marine Laboratory, Georgetown, SC 29442, and Marine Resources Research
Institute, South Carolina Department of Natural Resources, Hollings Marine Laboratory,
Charleston, SC 29412
11aMaryland Department of Natural Resources, Annapolis, MD 21401
12Department of Biological Sciences, Old Dominion University, Norfolk, VA 23529
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13Chesapeake Research Consortium, Edgewater, MD 21037

14Institute of Marine Science, University of Alaska Fairbanks, Fairbanks, AK 99775

Abstract

#
Corresponding author. Telephone: 410-221-8422; [email protected].
*Deceased
6bPresent address: Marine Sciences Research Center, Stony Brook University, Stony Brook, NY 11794
8bPresent address: Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 100 8th Ave. S., St.
Petersburg, FL 33701
10bPresent address: National Oceanic and Atmospheric Administration, 1305 East West Highway, Silver Spring, MD 20910
11bPresent address: National Oceanic and Atmospheric Administration, 1305 East West Highway, Silver Spring, MD 20910
 Heisler et al. Page 2

In January 2003, the US Environmental Protection Agency sponsored a “roundtable discussion” to

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develop a consensus on the relationship between eutrophication and harmful algal blooms (HABs),
specifically targeting those relationships for which management actions may be appropriate.
Academic, federal, and state agency representatives were in attendance. The following seven
statements were unanimously adopted by attendees based on review and analysis of current as well
as pertinent previous data: 1) Degraded water quality from increased nutrient pollution promotes
the development and persistence of many HABs and is one of the reasons for their expansion in
the U.S. and the world; 2) The composition – not just the total quantity – of the nutrient pool
impacts HABs; 3) High biomass blooms must have exogenous nutrients to be sustained; 4) Both
chronic and episodic nutrient delivery promote HAB development; 5) Recently developed tools
and techniques are already improving the detection of some HABs, and emerging technologies are
rapidly advancing toward operational status for the prediction of HABs and their toxins; 6)
Experimental studies are critical to further the understanding of the role of nutrients in HAB
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expression, and will strengthen prediction and mitigation of HABs; and 7) Management of nutrient
inputs to the watershed can lead to significant reduction in HABs. Supporting evidence and
pertinent examples for each consensus statement is provided herein.

Introduction
This report represents the synopsis of a “roundtable discussion” on the links between water
quality and eutrophication and the occurrence of harmful algal blooms (HABs). This
meeting, sponsored by the US Environmental Protection Agency (US EPA), was held in
Cambridge, Maryland, in January, 2003, and included academic experts as well as federal,
state and local agency representatives. The authors of this report represent all those in
attendance; our colleague, J. Heisler, who originated and guided development of the meeting
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and chaired the discussion group, is now deceased and this paper is contributed in his honor.

The goal of the meeting was to develop a set of consensus statements on presently
understood relationships between eutrophication and HABs, with particular emphasis on
implications for nutrient management programs. A broad definition (GEOHAB 2001) of
HABs was adopted for this purpose, including potentially toxic (auxotrophic, heterotrophic)
species and high-biomass producers that can cause hypoxia and anoxia and indiscriminant
mortalities of marine life after reaching dense concentrations, whether or not toxins are
produced.

In advance of the meeting, succinct statements for discussion were provided to participants
and a presentation was given on each statement by one member of the group. The presenter
was asked to make a case “for” or “against” the given statement. In discussion, and through
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analysis of data and evidence presented, the goal was to accept, reject, or modify each
statement so that a set of unanimously accepted statements were developed by the end of the
meeting. Statements were specifically crafted so as to have management implications. The
relevance and applicability for management of these consensus statements remain as valid at
present as when they were developed.

One recommendation from the roundtable was to develop a GEOHAB Open Science
Meeting on HABs and Eutrophication to broaden the discussion on this topic to a wider

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community of international participants. Such a meeting was held in 2005 and the scientific
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results from that meeting have been synthesized into a report (GEOHAB 2006) and some of
those results are further detailed in the other papers of this issue of Harmful Algae.

Herein, each consensus statement is summarized along with a synopsis of its rationale and
supporting evidence and a few examples. These synopses are not intended to be thorough
reviews. In keeping with the mission of the sponsoring agency for this roundtable, US EPA,
preference is given to US examples where available. It is recognized that, in some cases,
significant new data have become available since the 2003 roundtable. This report generally
uses the data presented in the roundtable and provides new data where advancements in the
field have been substantial.

The Consensus Statements

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1. Degraded water quality from increased nutrient pollution promotes the development and
persistence of many HABs, and is one of the reasons for their expansion in the U.S. and
other nations
It is generally recognized that there have been more algal blooms, often of greater
geographic extent and/or longer duration, with more toxic species observed, more fisheries
affected, and higher associated costs with HABs in the past decade than in previous decades
(Anderson 1989, Smayda 1990, Hallegraeff 1993, Anderson et al. 2002, Glibert et al.
2005a). Many possible reasons for the reported global expansion exist in addition to nutrient
pollution. Species dispersal or introduction, through transport of cells or cysts can occur via
natural currents and storm or human activities such as dispersal of ballast water exchange or
shellfish seeding operations by which algal cells or cysts may be transported. Both
overfishing and increase aquaculture alter food webs which may, in tur, alter the community
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of grazers that feed on HABs. Finally, improved observation and tools for detection have
increased public and scientific awareness (GEOHAB, 2001, HARRNESS, 2005). More than
one cause is frequently involved, and the causes for global expansion of a given species can
differ among species.

There are numerous examples worldwide of increases in HABs linked to increased nutrient
loading, a few of which are highlighted here. While strong relationships have been shown
for many years in freshwater ecosystems between phosphorus loadings and harmful
cyanobacteria blooms (Schindler, 1977 and Burkholder 2002), increasing linkages between
nutrient loading and estuarine/coastal marine HABs have more recently been recognized
(Smayda, 1990, Smayda, 1997, Anderson et al., 2002, Glibert et al. 2005a, and Gilbert and
Burkholder, 2006). For example, in the Gulf of Mexico, the sedimentary record of
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concentration of potentially toxic diatoms, Pseudo-nitzcschia spp., increased in parallel to

increased nitrate loading over the past several decades (Fig. 1; Turner and Rabalais, 1991,
Parsons et al., 2002). In Puget Sound, Washington, USA, a strong correlation has been
reported between the increase in documented levels of paralytic shellfish toxins (PST) from
toxic dinoflagellates over four decades and the increase in human population in the counties
bordering Puget sound (based on US census statistics; Fig. 2; Trainer et al., 2003). Although,
as above, a statistical correlation does not establish a causal link, this relationship suggests
that coastal eutrophication may be a causative agent of change (Trainer et al., 2003). Blooms

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off the coast of China, involving Prorocentrum sp., Karenia mikimotoi and other species,
have expanded during recent years in geographic extent and duration, from km2 to tens of
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km2, and from days to months, related to the increase in fertilizer use over the past two
decades (Fig. 3; Anderson et al., 2002 and Zhou, 2005). The Baltic Sea, Aegean Sea,
Northern Adriatic, and Black Seas have all sustained increases in HABs coincident with
increases in nutrient loading (e.g., Larsson et al., 1985, Bodenau, 1993 and Moncheva et al.,
2001). On a shorter time scale, Beman et al. (2005) reported, during a 5-year study, a strong
positive relationship between nitrogen-rich agricultural runoff to the Gulf of California and
the development, within days, of extensive phytoplankton blooms. In Sequim Bay,
Washington, an intense bloom of the toxigenic diatom Pseudo-nitzschia pseudodelicatissima
was found a week after elevated ammonium levels were reported in these waters (Trainer et
al., 2007), and similarly, in Chesapeake Bay, blooms of Prorocentrum minimum have been
found to follow within days of elevated levels of urea following agricultural applications
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(Gilbert et al., 2001).

Although such examples, supported by experimental and physiological data (e.g., Riegman,
1995, Bates et al., 1998, Imai et al., 1998, Smayda, 1998, Johansson and Granéli, 1999, Li et
al., 2001, Fan et al., 2003 and Glibert et al., 2006b), are increasing, recognition that
degraded water quality from nutrient pollution contributes to the development and
persistence of many HABs does not diminish the possibility that other factors may promote
some HABs. Physical, biological, and other chemical factors may modulate harmful algal
species’ responses to nutrient loadings (e.g., Vadstein et al., 2004, Gobler et al., 2002,
Sellner et al., 2003 and Glibert et al., 2005a), and this complexity of HAB dynamics is a
challenge for their management, as further described below.

2. The composition – not just the total quantity – of the nutrient pool impacts HABs
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Specific algal species or species groups have numerous physiological adaptations that permit
them to exploit nutrients differentially. Different species groups display preferences for
specific nutrient regimes, including nutrient ration or form (Smayda, 1990, Smayda, 1997,
Anderson et al., 2002, Smayda and Reynolds, 2001, Smayada and Reynolds, 2003 and
Glibert and Burkholder, 2006). For example, diatoms require silicon for their growth,
whereas certain dinoflagellates apparently have a higher phosphorus requirement than some
other species groups. Thus, according to the nutrient ratio hypothesis (Tilman 1977;
Smayda, 1990, Smayda, 1997), if nutrient loading leads to a proportional enrichment of
phosphorus relative to silicon, then a proportional shift away from a diatom-dominated
community toward flagellates might be expected over time.

The relationship between alteration in nutrient composition and the development of HABs is
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supported by examples in freshwaters, estuaries and marine coastal waters worldwide

(reviewed by Anderson et al. 2002). Off the coast of Germany, time series analysis of
nutrient concentrations over several decades showed that a 4-fold increase in the N:Si ratio
coincided with decreased abundance of diatoms and an increase in Phaeocystis blooms
(Radach et al., 1990). Similarly, a nearly 4-decade time series from Narragansett Bay shows
a relationship between increases in the N:Si ratio and a proportional increase in flagellates
(Smayda et al., 2004). Decreases in N:P ratios due to phosphorus loading have sometimes

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been related to increased abundance of certain harmful dinoflagellate species. For example,
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in Tolo Harbor, Hong Kong, where phosphorus loading increased due to human population
growth in the late 1980s, a shift from diatoms to dinoflagellates was observed, coincident
with a decrease in the ambient N:P ratio from ca. 20:1 to <10:1 (Hodgkiss and Ho, 1997 and
Hodgkiss, 2001). On shorter time scales, in Tunisian aquaculture lagoons, blooms of toxic
dinoflagellates have been shown to develop when the N:P ratio drops in autumn (Romdhane
et al., 1998), and along the eastern seaboard of the US, outbreaks of the toxic
dinoflagellates, Pfiesteria piscicida and P. shumwayae, have been associated with low N:P
ratios from high phosphate loading by effluent spills from concentrated animal operations
(Burkholder et al., 1997). Blooms of Karenia brevis on the western Florida shelf are also
found in waters with lower dissolved inorganic N:P ratios than in water directly to the south
with higher N:P ratios, where diatoms tend to be more prevalent (Fig. 4, Heil et al., 2007).

The impacts of varying nutrient composition on HAB proliferation, however, are in many
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cases more complicated than the examples. Some studies have shown, for example, that
neither the quantity nor the ratio of inorganic nutrients alone can adequately explain
sustained high biomass blooms of extended duration (e.g., Vargo et al., 2004). We now
recognize that inorganic nutrients are not the only nutrients used by many HABs, and that
many organic nutrients are bioavailable and dynamic in their composition (e.g., Seitzinger et
al., 2002 and Berman and Bronk, 2003). Many HAB genera, including dinoflagellates,
cyanobacteria, and pelagophytes (e.g., brown tides), can use organic (dissolved or
particulate) forms of nutrients for some or all of their nitrogen, phosphorus and/or carbon
demands (e.g., Paerl, 1988, Burkholder and Glasgow, 1997, Granéli et al., 1997, Granéli et
al., 1999, Berg et al., 1997, Berg et al., 2002, Stoecker, 1999, Kudela and Cochlan, 2000,
Berman, 2001, Glibert et al., 2001, Glibert et al., 2006a, Glibert et al., 2006b, Glibert et al.,
2007, Lomas et al., 2001, Lomas et al., 2004, Mulholland et al., 2002, Mulholland et al
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2004, Gobler et al., 2005, Glibert and Legrand, 2006, Kudela et al. 2008 and Cochlan et al.,
2008).

Nutrient “packaging” can also be important. For example, many flagellate species, including
various harmful dinoflagellates, are mixotrophic or heterotrophic phagotrophs, and consume
predominantly particulate rather than dissolved nutrients (e.g., Nygaard and Tobiesen, 1993,
Stoecker et al., 1999, Parrow and Burkholder, 2003, Jeong et al., 2005). Thus, the toxic,
heterotrophic dinoflagellate Pfiesteria spp. can be indirectly stimulated by inorganic nutrient
enrichment, mediated through an increase in the abundance of algal prey that may be
directly stimulated by specific nutrient forms (Burkholder et al., 2001, Glibert et al., 2006a).
Similarly, Karlodinium veneficum may be stimulated by the growth of cryptophytes which
may be stimulated by its preferred nutrient forms (Adolf et al., this issue).
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Furthermore, some cyanobacteria also have the ability to convert or “fix” gaseous nitrogen
into ammonia, enabling them to succeed in nitrogen-depleted conditions if other
environmental conditions permit their growth (Howarth et al., 1988). The dynamics of
nitrogen fixation by the cyanobacterium Trichodesmium have been related to increases in
dissolved organic nitrogen that is released from the cyanobacteria and which may be
available for subsequent uptake by dinoflagellates (e.g. Capone et al., 1994, Glibert and
Bronk, 1994, Glibert and O’Neil, 1999, Lenes et al., 2001, Mullholland et al., 2004). Thus,

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nutrient ratios based solely on dissolved inorganic nutrients often do not yield sufficient
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insights about influences of nutrient enrichment.

Toxin production may also vary with nutrient form. For example, laboratory studies have
revealed that the neurotoxin domoic acid (DA) production by the diatom Pseudo-nitszchia
spp. can vary as a function of the nitrogen substrate being utilized for growth. For
exponentially growing cultures of P. australis, nitrate and ammonium-grown cells produce
equivalent amounts of dissolved and particulate DA, whereas DA production is enhanced in
cultures growing solely on urea (Cochlan et al., 2005, Armstrong-Howard et al., 2007).
However, for the smaller-celled species, P. cuspidata, the nitrate-grown cells are the most
toxic (Auro, 2007).

In addition to macronutrients, micronutrients such as trace metals are essential for the
growth of all phytoplankton and play critical roles in both photosynthesis and assimilation of
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essential macronutrients, and the toxicity of some HAB species (Sunda, 2006). For example,
laboratory studies have shown that the toxigenic diatoms Pseudo-nitszchia multiseries and P.
australis produce increasing amounts of DA as a function of iron or copper limitation (Rue
and Bruland, 2001, Maldonado et al., 2002 and Wells et al., 2005). Additionally, it has been
seen that DA production in these diatoms increases under high copper concentrations,
presumably to detoxify copper (Maldonado et al., 2002, Ladizinsky, 2003 and Ladizinsky et
al., 2005). Iron, besides being essential for phytoplankton growth and nitrogen assimilation,
is also required for nitrogen fixation, and therefore the deposition of iron-rich dust in the
Gulf of Mexico has been related to the strength of Trichodesmium blooms and, indirectly, to
subsequent K. brevis blooms (e.g., Lenes et al., 2001).

In summary, nutrient preferences by different algal species groups are strongly supported by
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physiological evidence and by recognition of an array of adaptive mechanisms used by

different species. The extent to which these adaptations are expressed depends on other
environmental conditions at the time of nutrient supply, the types of nutrient supplied and
other factors. The inability to apply a single criterion, such as the nutrient ratio, to an
assessment of phytoplankton species dominance does not negate the utility of this approach;
rather, it underscores the complexity of physiology of many HAB species and the
interdependence of environmental factors in the outcome of any species succession (Glibert
and Burkholder, 2006).

3. High-biomass blooms must have exogenous nutrients to be sustained

Algal proliferations, by definition, are due to increased net growth, and this must be
accomplished either through increases in gross growth rate and/or through reductions in loss
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processes such as grazing (Harris, 1986). “New” nutrients from allochthonous sources can
fuel biomass increases. While increased total algal biomass is often an obvious response to
nutrient loading (see reviews in Cloern, 2001 and Anderson et al., 2002), the overall species-
specific response will depend upon the physiology of the organisms present, environmental
conditions, and the form of nutrient supplied, as described above. Clear dose-response
relationships between nutrient loading and biomass response (typically termed a “phase I”
eutrophication model sensu Cloern, 2001) are more common in lakes, however, than in
estuarine and marine systems.

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The relationships between nutrient loading and algal proliferations are complicated by shifts
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in food webs, habitat changes, climate changes and other system alterations that affect the
extent to which a given species may accumulate (typically termed a “phase II” model of
eutrophication; Cloern, 2001). Increased nutrient enrichment can lead to a shift in plankton
community composition, which in turn can afect predator–prey relationships, further altering
the transfer of nutrients (e.g., Smayda, 1989, MacIntyre et al., 2004, Irigoien et al., 2005,
Mitra and Flynn, 2006 and Sunda et al., 2006). Incoming nutrients may be regenerated,
recycled, or removed in space and time from the set of conditions that would otherwise
support blooms. These links are frequently difficult to establish.

Inside blooms, ambient concentrations of inorganic nutrient forms may be reduced or

depleted due to algal incorporation of the nutrients into biomass (e.g., Vargo et al., 2004 and
Springer et al., 2005), leading to relationships between nutrient concentration and
chlorophyll (or other biomass indicator) that may, in fact, appear to follow a saturation
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response, a negative relationship, or no relationship at all. Thus, the critical term is the flux
of nutrient, not the absolute concentration that may be supporting the blooms.

The most complex nutrient sources to understand and regulate are non-point source inputs
such as runoff, groundwater and atmospheric deposition. The relationship between increased
exogenous inputs and increased algal biomass is often clearer over long time periods.
Nitrogen loading, for example, in the Chesapeake Bay, which increased more than 2.5-fold
from the mid-1940s to the mid-1990s, has been correlated with long-term increases in total
chlorophyll, in the frequency and abundance of blooms of HAB species such as P. minimum,
and in resulting hypoxic volume (Hagy et al., 2004 and Kemp et al., 2005).

While exogenous nutrients are often necessary for high biomass blooms to be sustained, in
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some cases, blooms may be sustained on nutrients that are regenerated and recycled after an
initial injection of new nutrients. Long-term sustained blooms, such as the bloom of
Aureoumbra lagunensis evident in Laguna Madre for approximately 8 years in the 1990s,
and the >20 month bloom of K. brevis that was sustained off western Florida in 2005, appear
to have been fueled by an initial injection of nutrients, and then sustained on regenerated
nutrients. In the former case, intense rains after years of drought led to a sequence of blooms
and ecosystem conditions suitable for Aureoumbra (e.g., Buskey et al., 2001), while in the
latter case, a series of hurricanes in preceding months may also have altered both nutrient
availability and other habitat considerations (Mallin and Corbett, 2006 and Neely et al.,
2006). A third such example is that of the >18 months bloom of Synechococcus in eastern
Florida Bay that followed an injection of phosphorus from two apparent sources: high
freshwater discharge from Hurricanes Katrina, Rita and Wilma that impacted south Florida
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in 2005, and a very high organic loading from a unique situation of road construction that
required mulching of significant amounts of mangroves (Madden, in press). Consequently,
chlorophyll concentrations rose and were sustained at levels roughly eightfold higher than
pre-bloom levels, while an increase in phosphorus concentration was only observed during
the initiation stages of the bloom and then declined. A final example comes from brown
tides (Aureococcus anophagefferens) in US mid-Atlantic estuaries (Gobler et al., 2005).
These blooms are often preceded by a ‘pre-bloom’ of other algal species that are stimulated
by nitrogen from groundwater flow (Gobler and Sañudo-Wilhelmy, 2001). When

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groundwater flow diminishes during summer and the initial bloom is remineralized, organic
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nitrogen levels increase, and A. anophagefferens becomes the dominant alga. Thus, nutrients
may continue to serve as fuel for blooms long after the initial nutrient loading occurs.

4. Both chronic and episodic nutrient delivery promote HAB development

As described in some of the previous examples, the response of harmful algal species to
changes in nutrient enrichment is often a chronic effect, becoming increasingly apparent
only after long time intervals are examined (e.g., Lam and Ho, 1989, Smayda, 1989,
Riegman et al., 1993, Yung et al., 1997 and Marshall et al., 2005). Long-term, consistent
monitoring records additionally can reveal relationships between harmful algal species
composition and abundance versus other aspects of environmental change, such as climate
variability or alterations in trophic control due to changes in dominant herbivorous species.
Such long-term records are valuable in clarifying trends in nutrient loadings, and in
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identifying synergistic effects of changing climatic factors and nutrient enrichment (e.g.,
Smayda et al., 2004, Burkholder et al., 2006).

Episodic or “pulsed” nutrient inputs have also been related to outbreaks of harmful algal
species on both small and large scales. Some of these, such as agricultural applications
(timing and quantity), treated sewage discharge, and combined sewer outfalls, are amenable
to management. As examples (reviewed in Harlin, 1993), in Boston Harbor, sea lettuce
(Ulva) formed dense populations for many years near outfalls of poorly treated sewage.
Along the intertidal area of the Baltic Sea, sewage inputs have been related to overgrowth of
formerly dominant brown seaweeds (Fucus spp.) by opportunistic macroalgae. Episodic
inputs resulting from storm events are, naturally, more difficult to manage.

Episodic storm events and climate variability affect the timing of freshwater flow, residence
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times, the magnitude and timing of nutrient pulses and resulting biotic responses (e.g.,
Miller et al., 2006, Burkholder et al., 2006, Mallin and Corbett, 2006 and Paerl et al., 2006).
In coastal lagoons, where riverine input is not the dominant source of nutrient delivery,
climate variability can alter the input of groundwater nutrients (e.g., LaRoche et al., 1997).
Hurricane Isabel in 2003 caused a large phytoplankton bloom to develop in Chesapeake Bay
within days (Miller et al., 2005). Further, extensive hypoxia occurred in the lagoonal Neuse
River Estuary after Hurricanes Dennis and Floyd, whereas a storm that caused less flooding,
Hurricane Fran, led to more concentrated pollutants, extensive anoxia and massive fish kills
(Burkholder et al., 2006). In the Choptank River subestuary of Chesapeake Bay, annual
spring blooms of P. minimum generally follow within days of spring agricultural application
of nitrogen fertilizer and its runoff from episodic spring rains (Glibert et al., 2001).
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In some cases anthropogenic nutrients may not directly stimulate HABs, but may become
linked to their growth and abundance following biogeochemical processing or following the
stimulation of other components of the food web on which they may depend.

On a seasonal scale in Chesapeake Bay, USA, nutrient input in the spring is delivered largely
in the form of nitrate and rapidly assimilated by diatoms which bloom, then sink and
decompose as nutrients become depleted. Subsequently during warmer summer months,
nitrogen, largely as ammonium, is released via decomposition in sedimentary processes

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which, in turn, supports an assemblage dominated by flagellates including potentially

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harmful dinoflagellates (Glibert et al., 1995, Malone et al., 1996 and Kemp et al., 2005).

It is thus important in our interpretation of the relationships between nutrients and HAB
occurrences that we move away from simplistic inorganic nutrient-dose-yield models and
begin to incorporate nutrient loading parameters which encompass the increasing array of
nutrient forms that are now recognized to be important. Furthermore, interpretations of
nutrient effects on HABs as well as models that parameterize these relationships, need to
incorporate indirect, time-lagged nutrient pathways, as well as the feedbacks and
interactions of the effects of nutrient loads in ecosystems (Cloern, 2001).

5. Recently developed tools and techniques are already improving the detection of some
HABs, and emerging technologies are rapidly advancing toward operational status for the
prediction of HABs and their toxins
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Due to the unpredictability of most episodic events, sampling programs historically have not
“captured” the initiation phases of blooms. However, new in situ monitoring tools are
beginning to permit resolution of the antecedent conditions and the time course response to
some episodic events. Improved molecular probes, some that can be incorporated into in situ
microarrays, are allowing timely detection of cells. Molecular probes for individual HAB
species and their toxins are now routinely applied for many species, making early detection
possible (e.g., Scholin and Anderson, 1998, Scholin et al., 2003, Anderson et al., 2005a and
Bowers et al., 2006). Optical sensors for Karenia species have been deployed on moorings
and autonomous underwater vehicles (Schofield et al., 1999). In situ probes with telemetry
for various key variables such as temperature, salinity, chlorophyll, turbidity, dissolved
oxygen and pHs are also providing near-real time data for management applications
(Glasgow et al., 2004 and Springer et al., 2005). A suite of over 50 such probes in the State
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of Maryland are allowing managers and the public alike to monitor trends in Chesapeake
Bay and rapidly respond when conditions warrant (www.eyesonthebay.net). In situ nutrient
sensors are also advancing, with capability developing for some organic forms of nutrients
as well as inorganic forms, so that relationships between pulses in nutrient delivery and
alterations in salinity due to rainfall, for example, are now possible to establish (Glibert et
al., 2005b and Glibert et al., 2008).

In conjunction with the growing sophistication of tools, better citizen awareness and citizen
monitoring can also be effective in capturing blooms or blooms conditions. Throughout the
US and in many parts of the world, fishermen collect samples for cell and nutrient analyses,
and local citizen groups and indigenous people participate in routine monitoring (e.g.,
Scaefer et al., 2004, Trainer and Suddleson, 2005, Whereat and Farestad, 2005 and Granéli
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and Esplund, 2006).

Modeling is a rapidly developing tool advancing toward prediction of many HAB species
and occurrences (e.g., Flynn, 2002, McGillicuddy et al., 2005 and Hood et al., 2006),
although for most estuarine and coastal HABs, prediction has not yet been attained (see, e.g.,
Franks, 1997, Cembella, 1998 and Flynn, 2005). There are two general types of HAB
models that are useful for management applications. The first is the development of models
that predict “general likelihood of occurrence” of HAB species, whereas the second is the

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development of models that include “explicit” predictions of HAB occurrence in time or

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space. The former is useful for management in application of long-term actions to reduce the
likelihood of future occurrences, i.e. prevention. The latter requires more refinement to
understand the physics, biology and chemistry of the environment, but it can be of more
value at the local community level. Models of a range of types are useful in predicting
general likelihood of occurrence, from simple regression models that may yield correlation
(without necessarily a biological foundation for cause and effect) and conceptual models that
are useful in communicating general patterns (e.g., Smayda and Reynolds, 2001 and Smayda
and Reynolds, 2003). In advancing toward more explicit predictions, mechanistic models
that describe the physical, chemical and biological interactions are required. Spatially
explicit models linked to hydrodynamic models are yielding some success in retrospectively
tracking some species, such as for Alexandrium spp. in the Gulf of Maine and K. brevis in
the Gulf of Mexico (McGillicuddy et al., 2005, Walsh et al., 2006). Multi-parameter
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physiological models that incorporate various organismal life stages and trophic interactions
are also beginning to be developed (J. Anderson et al., 2003; D. Anderson et al., 2005b and
Hood et al., 2006).

The development of explicit, reliable model predictions still needed for most HABs will
require significant data on the species of interest as well as the environmental conditions
(Flynn, 2002 and Flynn, 2005). Thus, for some species, “general likelihood” predictions are
viable now and can be useful in guiding long-term management decisions with respect to
nutrients. Furthermore, several types of real-time and near-real-time monitoring systems,
coupled with conceptual, statistical, or mechanistic models, are also available now to assist
in detecting and predicting some HABs in time and space. Now-cast models are being
developed in the Chesapeake, Bay, for example, of the likelihood for K. veneficum blooms
based on a statistical habitat relationship of the HAB with salinity and temperature, and a
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hydrodynamic model (Ramers et al., 2003 and Tango et al., 2005). However, the prediction
“window” for those species for which such mechanistic models are available is presently
short, and considerable work will be needed to strengthen insights about the relationships
between nutrient responses, physical dynamics, and climate change. Application of real-time
monitoring of both environmental parameters and HABs species will continue to advance
forecasting capabilities for these dynamic relationships.

6. Experimental studies are critical to further understanding about the role of nutrients on
HAB expression, and will strengthen prediction and mitigation of HABs
Many physiological adaptations to nutrients are best examined under controlled laboratory
conditions. For example, assessments of specific relationships that are required in models
(such as parameters of nutrient uptake and growth kinetics) are better resolved under
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laboratory conditions where a culture of known physiological state can be established and
where environmental conditions can be rigorously set (e.g., Lomas et al., 1996, Fan et al.,
2003, Glibert et al., 2006b, Herndon and Cochlan, 2007 and Cochlan et al., 2008).
Laboratory culture studies of HAB species have been instrumental in resolving such species
characteristics as life histories, toxigenesis, ecophysiological responses to specific nutrient
forms, light and temperature regimes, and species-specific differences in rates of nutrient
uptake and growth. As new insights are developed about various processes – for example,

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 Heisler et al. Page 11

the extent of osmotrophy or mixotrophy within a species – generalizations based upon older
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laboratory data may have to be revisited, cross-confirmed, or assessed anew.

A critical but often overlooked consideration regarding experimental work is that major
characteristics of species maintained in culture for extended periods (months to years)
significantly change over time under (highly artificial) enclosed conditions. Over time in
culture, highly toxic strains have lost their ability to make toxin; strains also have changed in
polyploidy, expression of life history stages, and responses to environmental conditions such
as salinity and nutrient regimes (reviewed in Wood and Leatham, 1992 and Burkholder and
Glibert, 2006). Pfiesteria spp., for example, have been shown to lose their toxicity when
switched from a media that includes live to one with algal prey (Burkholder et al., 2001).
Toxin production in a strain of Alexandium lusitanicum was also shown to loose toxicity
after many years in culture, and although the exact reasons could not be ascertained, genetic
mutations or prolonged use of antibiotics may have been the cause (Martins et al., 2004).
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Many species have shown strain differences unrelated to extended period in culture. For
example, Strom and Bright (2003) observed that strains of the haptophyte Emiliania huxleyii
varied in their response to different forms of nitrogen. Whereas all four strains tested grew
on nitrate and ammonium, three of the four could grow on organic nitrogen sources, while
the fourth could not. The strains also showed distinct responses to various forms of organic
nitrogen. Thus, in conducting laboratory studies, the history of the culture should be
carefully considered (e.g., location of isolation and duration in culture). It is also important
to compare multiple strains of the same species to assess whether the characteristic of
concern is strain-specific, and generalizations at the species level (or higher) based upon one
to a few strains should be avoided (Burkholder and Glibert, 2006, Burkholder et al., 2001
and Burkholder et al., 2005).
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Experiments should continue to build upon the knowledge gained from unialgal culture
studies to assessment of more complex systems with multiple species, from microcosms to
mesocosms, and from laboratory studies to field trials. Mesocosm studies and field
experiments, if carefully designed and controlled, can enable in situ assessment of processes
of trophodynamics and community interactions with individual species (e.g., Stoecker and
Gustafson, 2002), and the importance of environmental fluctuations in light, temperature,
and community-level responses to nutrient enrichment. Such approaches have significantly
advanced understanding of nutrient limitation. As examples, the classic whole-lake studies
undertaken decades ago in Canada yielded tremendous insights about phosphorus limitation
in freshwater systems (Schindler, 1987 and Schindler, 2006). Analogously, much was
learned about the regulation of marine phytoplankton production by iron in the multiple in
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situ iron enrichment experiments conducted in the high-nutrient-low-chlorophyll (HNLC)

regions of the world (reviewed by de Baar et al., 2005). Smaller-scale mesocosms also have
helped to resolve nutrient preferences by the harmful brown tide species, A. anophagefferens
(Kana et al., 2004) and the effects of trophic structure on top-down regulation of
phytoplankton biomass (Glibert, 1998, Granéli and Turner, 2002, Buskey et al., 2003 and
Vadstein et al., 2004).

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 Heisler et al. Page 12

As model sophistication and insights continue to develop about the dynamic regulation of
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adaptive characteristics of individual species, there will be a ongoing need to experimentally

document specific processes under controlled conditions with clonal algal isolates, both as
individual species (±bacteria, e.g., Bates et al., 1995 and Burkholder et al., 2005) and as
mixes of species in an increasingly complex but controlled environment (e.g., Flynn, 2002).
Based upon the major insights gained from previous experiments, the data from such
controlled conditions will surely strengthen scientists’ abilities to predict and mitigate
HABs.

7. Management of nutrient inputs to the watershed can lead to significant reductions in

HABs
There are now multiple examples demonstrating both total algal biomass and HAB
occurrence decreases after reduction in nutrient input. One of the classic examples involving
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decreases in cyanobacterial blooms is that of the removal of sewage discharges from Lake
Washington within metropolitan Seattle, Washington (Edmondson, 1970). This lake had
sustained noxious cyanobacteria blooms from the 1920s through the 1960s because of raw
sewage inputs. An elimination of sewage discharges to Lake Washington was imposed in
1968, and the cyanobacterial blooms declined. In a much larger system, Lake Erie, the green
macroalga Cladophora had choked much of the west basin with massive growth until
improved wastewater treatment and detergent phosphate bans in the early 1980s led to
significant reduction in the nuisance blooms (Ashworth, 1986). Reduced nutrient loading
similarly has promoted declines in estuarine and marine coastal HABs. Sewage discharges to
Mumford Cove, a shallow estuary in Connecticut, were re-routed to another waterway in the
late 1980s, and within 2 years massive nuisance blooms of the macroalga, Ulva lactuca,
were eliminated (Harlin, 1993). In the Potomac River, a tributary of Chesapeake Bay,
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phosphate removal from sewage in the late 1970s was related to significant reductions in the
frequency and intensity of Microcystis blooms that had been problematic in the previous
decade (Jaworski, 1990). In the Seto Inland Sea in Japan between 1965 and 1976, the
number of red tide outbreaks (high biomass blooms) increased sevenfold (Okaichi, 1997), in
parallel with the increase in industrial production, but in 1973, Japanese authorities instituted
the Seto Inland Sea Law to reduce loadings to half of the 1974 levels over a 3-year period.
The number of red tides began to decrease in 1977, eventually falling to less than 30% of the
peak frequency, which had been in excess of 300 blooms year−1(reviewed by Imai et al.,
2006).

A more recent example appears to be that of the Long Island brown tides which, while so
common in the early 1990s, were virtually absent from the Long Island embayments through
the middle of the following decade (Fig. 5; Gobler et al., 2005). Although multiple factors
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have been suggested to be related to the decline in bloom intensity, the recent reductions in
nitrogen levels in Peconic Estuary have been correlated with these declines (Nuzzi and
Waters, 2004 and Gobler et al., 2005). Blooms of A. anophagefferens are generally reliant
on organic sources of nitrogen for growth (Dzurica et al., 1989, Lomas et al., 1996, Berg et
al., 1997, Berg et al., 2002, Mulholland et al., 2002 and Mulholland et al., 2004). In the
Long Island embayments, the organic sources fueling these blooms are not thought to be a
direct external nutrient source, but rather derive from the internal processing of other “new”

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 Heisler et al. Page 13

nitrogen sources, including groundwater flow, which is elevated in nitrate. This nitrate
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delivery supports blooms of diatoms, as well as blooms of benthic microalgae which, as they
begin to dissipate, can supply the necessary organic nitrogen for the brown tide (Gobler and
Sañudo-Wilhelmy, 2001, MacIntyre et al., 2004 and Gobler et al., 2005). From 1995 to
2006, levels of DON declined substantially and brown tides were absent from the Peconic
Bays during those years (Gobler et al., 2005). In sharp contrast, however, in Maryland
embayments, where brown tide also blooms, organic nutrient concentrations have been
increasing annually over the past decade, leading to more significant blooms each year over
the decade from the mid-1990s to the mid-2000s (Trice et al., 2004 and Glibert et al., 2007).

Although these specific examples suggest that some successes may be possible in reducing
incidences of HABs by reducing nutrient inputs, for many species these relationships may
be complex. Long time scales may be involved, due to long-term storage of nutrient in
sediments and alteration in the biogeochemistry of systems after years of nutrient loading
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(e.g., Kemp et al., 2005). Furthermore, for some systems, ecosystem dynamics may be
permanently altered, and nutrient reduction strategies alone will not yield original ecosystem
conditions. Eutrophication stressors such as loss of benthic habitat, development of hypoxia/
anoxia, and alterations in food webs (Cloern, 2001) require long time scales for restoration
and may require changes at the landscape scale.

With increasing pressures on the coastal landscape, it must be underscored that prevention of
large blooms through nutrient control is far preferable than attempts to eradicate HABs once
they are established. It is, however, a significant challenge and extremely costly to enact
such policy decisions on large-scale nutrient reductions, so there will continue to be pressure
to develop bloom control strategies. Furthermore, different nutrient actions may be required
for different types of HABs, and organic as well as inorganic nutrients must be considered.
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Effective management is an iterative process, involving adaptive management as new

knowledge is gained, and must be sustained to be effective. Lastly, timely communication of
results, to stakeholders and the public, is critical. Given projected increases in human
population worldwide, eutrophication pressures and increased HAB occurrences will
undoubtedly continue to increase in years to come.

Acknowledgments
The “roundtable” discussion which forms the basis of this paper was funded by the US EPA. Meeting support was
provided by Battelle. J. Hawkey assisted with logistics and graphics. PMG’s time to prepare this manuscript was
provided by grant NAO4NOS4780241 from NOAA MERHAB. This is contribution number 4120 from the
University of Maryland Center for Environmental Science and MERHAB contribution number 58. [SS]

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Figure 1.
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).
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Figure 2.
Relationship between the growth in human population (and presumably their nutrients) and
HABs from Puget Sound, Washington State, where continuous monitoring of paralytic
shellfish poisoning has been ongoing since the mid-1950’s. Plotted here is the relationship
between human population in the region for the past 40 years (data were derived from the
U.S. census) and the average decadal maximum recorded amount of paralytic shellfish
toxins, PST (redrawn from Trainer et al. 2003).
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Figure 3.
Long term trends in the use of nitrogen based fertilizers and the number of occurrences of
red tide blooms in Chinese coastal waters (modified and redrawn from Anderson et al. 2002
and Zhou et al. 2005).
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Figure 4.
Mean dissolved inorganic and organic N:P ratios for each of the major riverine systems of
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western Florida shelf sampled during the dry season of May 2004. Each bar represents the
means of the stations sampled along an individual riverine transect. The insert box indicated
the mean particulate N:P ratio. The general zones are indicated on the companion map of
southern Florida (modified from Heil et al. 2007).
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Figure 5.
Long- term trends in brown tide in Peconic Estuary Long Island (open bars) and in
Maryland Coastal Bays (closed bars; redrawn from Gobler et al. 2005 and Glibert et al.
2007).
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