Toxicity from other compounds (allelopathy)
Many of the bloom-forming species produce other compounds that are toxic to other members of the plankton,
whether other phytoplankton taxa that compete for nutrients and sunlight in active growth or potential grazers that
could limit accumulation. These compounds are “toxic” in
that they provide the bloom former greater opportunity for
maintaining growth, while their competitors and predators
are limited in their ability to lower their growth rates or
accumulation. Referred to as allelopathic compounds,
several bloom taxa produce spectrums of compounds with
these properties. Examples include Karenia brevis, the
Florida red tide taxon, which produces compounds that
kill two competing diatoms and a dinoflagellate (Prince
et al., 2008) and retard rotifer grazing on the dinoflagellate
(Kubanek et al., 2007). Alexandrium tamarense and
A. minutum produce compounds that had negative effects
on the diatom Thalassiosira weissflogii and the
cryptophyte Rhodomonas, as well as a natural community
and a ciliate (Fistarol et al., 2004). Cyanobacteria also produce inhibitory compounds, with Nodularia spumigena,
Aphanizomenon flos-aquae, and Anabaena lemmermannii
all inhibiting these same taxa (Suikkanen et al., 2004).
Another dinoflagellate, Cochlodinium polykrikoides,
inhibits the growth of Akashiwo sanguinea, Gymnodinium
instriatum, and Chattonella marina as well as members of
the natural phytoplankton community from Long Island
estuaries likely through production of reactive oxygen
species (Tang and Gobler, 2010); raphidophytes like
C. marina, C. antiqua, Fibrocapsa japonica, and
Heterosigma akashiwo have similar ROS production
capacities (Marshall et al., 2005). ROS production can
lead to gill damage in fish and death (Kim et al., 1999).
The prymnesiophyte Prymnesium parvum produces compounds inhibitory to several dinoflagellates (Fistarol et al.,
2003). Some macroalgae (Ulva, Corallina, Sargassum,
Gracilaria, many coral reef cyanobacteria) also produce
allelopathic compounds inhibitory to other phytoplankton
and macroalgae (Nagle and Paul, 1999; Wang et al., 2007;
Tang and Gobler, 2011).
Mechanisms for bloom formation
Planktonic blooms can originate from physical mechanisms (Sellner et al., 2003) like circulation patterns
(Langmuir cells, fronts, upwelling), local storms and
precipitation, poor mixing, stratification, limited flushing,
or periods of low nutrient but abundant light which favors
surface accumulations via positive phototactic swimming
or buoyancy control of several toxic species. Examples of
these physically driven aggregations of cells include frontal concentration of Gymnodinium in the Potomac River
estuary (Tyler and Heinbokel, 1985) and Gymnodinium
catenatum in Spanish Rias (Figueiras et al., 1995); blooms
of diatoms transitioning to dinoflagellates from windinduced upwelling of nutrient-rich deepwater in
mid-Chesapeake Bay (Malone et al., 1986; Sellner and
Brownlee, 1990); rainfall-induced fresher lenses of water
overlying salty, dense estuarine water (Loftus et al.,
1972); blooms of Microcystis in tidal fresh embayments
with little exchange (Linkov et al., 2007) or coastal
lagoons with limited flushing and long residence times
where raphidophyte or brown tide blooms are frequently
observed (Gobler et al., 2005; Handy et al., 2005); and
dense, water discoloring surface blooms of several dinoflagellates and gas vesicle-rich cyanobacteria in highly
stratified and nutrient-poor surface waters (e.g., Sellner
and Brownlee, 1990; Suikkanen et al., 2007).
The latter bloom populations have remarkable diel
behaviors afforded to them through motility from
flagella and gas vesicle buoyancy, respectively. Diurnal
surface aggregation is assured through active upward
swimming of the dinoflagellates via positive phototaxis
(Kamykowski et al., 1998), while in the cyanobacterium,
flotation is assured through filling of thick-walled gas
vesicles in the cell, causing the cells to rise to the surface.
At night, the dinoflagellates may actively swim or passively settle to depth, while the cyanobacterium, now rich
in carbohydrate from daylong photosynthesis, sinks due
to the carbohydrate ballast that overwhelms the buoyancy of the gas vesicles in the cyanobacterium. While at
depth, both groups assimilate nutrients. The dinoflagellates respond to daylight again, actively swimming to
the surface. In contrast, nocturnal respiration of the carbohydrate in the cyanobacterium oxidizes the carbohydrate, removing ballast, and buoyancy produced
through gas-filled vesicles again returns the cyanobacterium to the surface (e.g., Chu et al., 2007).
Finally, unique life cycles for some of the bloomforming species ensure continued growth opportunities
when light, nutrients, and physical conditions are
near optimal (see Fryxell, 1983). Many dinoflagellates
(e.g.,
Alexandrium,
Gonyaulax,
Protoceratium,
Peridinium, Diplopsalis, Diplopsalopsis, Diplopeltopsis,
and Scrippsiella) and raphidophytes (Heterosigma
akashiwo, Fibrocapsa japonica) produce temporary and
permanent resting stages (cysts) that on resuspension into
the overlying water column can excyst (burst from the
cyst wall) to resume the swimming behavior described
above. Similarly, some diatoms produce resting spores
(e.g., Chaetoceros, Leptocylindrus, Bacteriastrum),
enabling the same reemergence and growth possibilities.
For the cyanobacteria, some taxa (e.g., Aphanizomenon,
Anabaena) produce resting stages called akinetes and, like
cysts and spores, enable regrowth. Others (M. aeruginosa)
simply settle to the bottom in the fall to overwinter as neardormant populations on the sediment surface, only to be
resuspended in the late spring for reinitiating cell division
and accumulation into new blooms.
Summary
Toxic (and nontoxic) blooms of planktonic and benthic
single-cell organisms and accumulations of macroalgae
are increasingly common in the world’s nutrient-rich estuaries, symptomatic of eutrophication attributable to mass land
TOXIC BLOOMS
715
Many of the bloom-forming species produce other compounds that are toxic to other members of the plankton,
whether other phytoplankton taxa that compete for nutrients and sunlight in active growth or potential grazers that
could limit accumulation. These compounds are “toxic” in
that they provide the bloom former greater opportunity for
maintaining growth, while their competitors and predators
are limited in their ability to lower their growth rates or
accumulation. Referred to as allelopathic compounds,
several bloom taxa produce spectrums of compounds with
these properties. Examples include Karenia brevis, the
Florida red tide taxon, which produces compounds that
kill two competing diatoms and a dinoflagellate (Prince
et al., 2008) and retard rotifer grazing on the dinoflagellate
(Kubanek et al., 2007). Alexandrium tamarense and
A. minutum produce compounds that had negative effects
on the diatom Thalassiosira weissflogii and the
cryptophyte Rhodomonas, as well as a natural community
and a ciliate (Fistarol et al., 2004). Cyanobacteria also produce inhibitory compounds, with Nodularia spumigena,
Aphanizomenon flos-aquae, and Anabaena lemmermannii
all inhibiting these same taxa (Suikkanen et al., 2004).
Another dinoflagellate, Cochlodinium polykrikoides,
inhibits the growth of Akashiwo sanguinea, Gymnodinium
instriatum, and Chattonella marina as well as members of
the natural phytoplankton community from Long Island
estuaries likely through production of reactive oxygen
species (Tang and Gobler, 2010); raphidophytes like
C. marina, C. antiqua, Fibrocapsa japonica, and
Heterosigma akashiwo have similar ROS production
capacities (Marshall et al., 2005). ROS production can
lead to gill damage in fish and death (Kim et al., 1999).
The prymnesiophyte Prymnesium parvum produces compounds inhibitory to several dinoflagellates (Fistarol et al.,
2003). Some macroalgae (Ulva, Corallina, Sargassum,
Gracilaria, many coral reef cyanobacteria) also produce
allelopathic compounds inhibitory to other phytoplankton
and macroalgae (Nagle and Paul, 1999; Wang et al., 2007;
Tang and Gobler, 2011).
Mechanisms for bloom formation
Planktonic blooms can originate from physical mechanisms (Sellner et al., 2003) like circulation patterns
(Langmuir cells, fronts, upwelling), local storms and
precipitation, poor mixing, stratification, limited flushing,
or periods of low nutrient but abundant light which favors
surface accumulations via positive phototactic swimming
or buoyancy control of several toxic species. Examples of
these physically driven aggregations of cells include frontal concentration of Gymnodinium in the Potomac River
estuary (Tyler and Heinbokel, 1985) and Gymnodinium
catenatum in Spanish Rias (Figueiras et al., 1995); blooms
of diatoms transitioning to dinoflagellates from windinduced upwelling of nutrient-rich deepwater in
mid-Chesapeake Bay (Malone et al., 1986; Sellner and
Brownlee, 1990); rainfall-induced fresher lenses of water
overlying salty, dense estuarine water (Loftus et al.,
1972); blooms of Microcystis in tidal fresh embayments
with little exchange (Linkov et al., 2007) or coastal
lagoons with limited flushing and long residence times
where raphidophyte or brown tide blooms are frequently
observed (Gobler et al., 2005; Handy et al., 2005); and
dense, water discoloring surface blooms of several dinoflagellates and gas vesicle-rich cyanobacteria in highly
stratified and nutrient-poor surface waters (e.g., Sellner
and Brownlee, 1990; Suikkanen et al., 2007).
The latter bloom populations have remarkable diel
behaviors afforded to them through motility from
flagella and gas vesicle buoyancy, respectively. Diurnal
surface aggregation is assured through active upward
swimming of the dinoflagellates via positive phototaxis
(Kamykowski et al., 1998), while in the cyanobacterium,
flotation is assured through filling of thick-walled gas
vesicles in the cell, causing the cells to rise to the surface.
At night, the dinoflagellates may actively swim or passively settle to depth, while the cyanobacterium, now rich
in carbohydrate from daylong photosynthesis, sinks due
to the carbohydrate ballast that overwhelms the buoyancy of the gas vesicles in the cyanobacterium. While at
depth, both groups assimilate nutrients. The dinoflagellates respond to daylight again, actively swimming to
the surface. In contrast, nocturnal respiration of the carbohydrate in the cyanobacterium oxidizes the carbohydrate, removing ballast, and buoyancy produced
through gas-filled vesicles again returns the cyanobacterium to the surface (e.g., Chu et al., 2007).
Finally, unique life cycles for some of the bloomforming species ensure continued growth opportunities
when light, nutrients, and physical conditions are
near optimal (see Fryxell, 1983). Many dinoflagellates
(e.g.,
Alexandrium,
Gonyaulax,
Protoceratium,
Peridinium, Diplopsalis, Diplopsalopsis, Diplopeltopsis,
and Scrippsiella) and raphidophytes (Heterosigma
akashiwo, Fibrocapsa japonica) produce temporary and
permanent resting stages (cysts) that on resuspension into
the overlying water column can excyst (burst from the
cyst wall) to resume the swimming behavior described
above. Similarly, some diatoms produce resting spores
(e.g., Chaetoceros, Leptocylindrus, Bacteriastrum),
enabling the same reemergence and growth possibilities.
For the cyanobacteria, some taxa (e.g., Aphanizomenon,
Anabaena) produce resting stages called akinetes and, like
cysts and spores, enable regrowth. Others (M. aeruginosa)
simply settle to the bottom in the fall to overwinter as neardormant populations on the sediment surface, only to be
resuspended in the late spring for reinitiating cell division
and accumulation into new blooms.
Summary
Toxic (and nontoxic) blooms of planktonic and benthic
single-cell organisms and accumulations of macroalgae
are increasingly common in the world’s nutrient-rich estuaries, symptomatic of eutrophication attributable to mass land
TOXIC BLOOMS
715