Download TURNER, JEFFERSON T., AND PATRICIA A. TESTER. Toxic marine

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64 1997,
Ocmrogr..
42(5, part 2), 1997, 1203-1214
by the American
Society
of Limnology
and Oceanography,
Inc
Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs
JefSerson T. Turner
Biology Department, University
of Massachusetts Dartmouth, North Dartmouth, Massachusetts 02747-2300
Patricia A. Tester
National Marine Fisheries Service, NOAA, Southeast Fisheries Science Center, Beaufort Laboratory, Beaufort,
North Carolina 285 16-9722
Abstract
Interactions between toxic phytoplankton and their zooplankton grazers are complex. Some zooplanktcrs ingest
some toxic phytoplankters with no apparent harm, whereas others are deleteriously affected. Phycotoxins vary in
their modes of action, levels of toxicity and solubility, and affect grazers in different ways. Beyond effects on direct
grazers, toxins may accumulate in and be transfcrrcd through marine food webs, affecting consumers at higher
trophic levels, including fish, scabirds, and marine mammals. Grazers of toxic phytoplankton include protists as
well as metazoans, and the impact of zooplankton grazing on development or termination of toxic blooms is poorly
understood. In most interactions of toxic phytoplankters with grazers and other marine food-web components,
outcomes are situation-specific, and extrapolation of results from one set of circumstances to another may be
inappropriate.
Toxic or otherwise harmful phytoplankton blooms may be
increasing in frequency worldwide (Smayda 1989; Hallegracff
1993). Accumulation of phytoplankton toxins in shellfish with
subsequent poisoning of humans (Shumway 1990) and fish
kills (Steidinger 1983; Burkholder et al. 1995) are widely
known, However, interactions between toxic phytoplankters
and their zooplankton grazers, subsequent food-web transport
of toxins, and effects on pelagic consumers at higher trophic
levels are more obscure. Phycotoxin transport through food
webs is indicated by mortality of whales, dolphins, and sea
birds following ingestion of phycotoxins (Anderson and White
1992; Gerachi et al. 1989; Work et al. 1993).
The reasons for phytoplankton toxin production are not
clear. Just because phytoplankters are toxic dots not mean
neccessarily that toxicity evolved to repel grazers. Indeed,
certain zooplankton ingest various toxic phytoplankters with
impunity, whereas for others, deleterious effects may result.
Putative explanations for toxicity other than grazing deterrence include precursors for subcellular organelles (Baden et
al. 1979), cell-wall degradation products (Kim and Martin
1974), nucleic acid synthesis (Abbott and White 1979;
Yentsch 1981), nitrogen storage (Dale and Yentsch 1978), or
inhibition of competing, co-occurring phytoplankton species
(Freeberg et al. 1979; Windust et al. 1996). Within the phytoplankton-zooplankton community there are few examples
of toxins as grazing deterrents to compare with the coevolution between benthic marine grazers and antipredatory
chemicals in the plants they consume (Hay 1991). There are
only suggestions from studies of copepods (Turner and Tester 1989) and bivalve molluscs (Shumway and Cucci 1987)
that coevolutionary experience or periodic exposure to toxic
Acknowledgments
We thank Don Anderson, Dave Garrison, Kevin Sellner, Peter
Verity, and an anonymous reviewer for constructive criticism of
several earlier, longer versions of this review.
phytoplankton blooms may have conferred some ability to
consume toxic phytoplankton with no ill effects.
Much of the disparity of effects is due to the variety of
phytoplankton toxins. Among the approximately 20 phytoplankton genera known to be toxic (Taylor 1990), there is a
plethora of toxins with widely differing effects (see Steidinger 1983; Baden and Trainer 1993; Hallegraeff 1993) which
can vary with potency and concentration (Anderson et al.
1990, 1994; Cembella et al. 1988). Intracellular levels of
toxins can vary within a single algal clone, depending upon
culture age and conditions (Maranda et al. 1985; Baden and
Tomas 1988; Cembella and Therriault 1989; Bates et al.
1991, 1993; Flynn and Flynn 1995; see also Graneli et al.
1990; Smayda and Shimizu 1993; Lassus et al. 1995) or
presence of toxic intracellular bacteria (Kodama 1990; Doucette 1995). Variations in phytoplankton toxicity result in
complex and inconsistent interactions between toxic phytoplankters and their grazers. There is also variation in physiological responses of organisms to algal toxins in terms of
binding or recognition-the
initial event in the onset of toxicity (Baden and Trainer 1993). Most marine phycotoxins
influence neurotransmission or enzyme inhibition (Table 1).
Differences in affinity of binding sites or the degree of decentralization of invertebrate nervous systems may account
for the lack of apparent effect of some toxins.
Beyond effects on their immediate grazers, phytoplankton
toxins may be passed up the food web through zooplankton
and fish that serve as vectors for higher trophic levels. Other
than for ciguatera fish poisoning, there is little information
about this process, and it is difficult to assess the potential
for toxins reaching fish that could be consumed by humans.
Just as toxic phytoplankters have potential impact on zooplankton and other pelagic consumers, grazing can have potential impact on preventing or terminating blooms. An obvious implication of a large monospecific bloom is that
grazing control is out-of-balance with phytoplankton growth
and(or) physical concentration. Such an occurrence may be
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Turner and Tester
Table 1. Characteristics of phytoplankton
Toxin
toxins.
Characteristics
Mode of action
Brevetoxin
Na’ channel activator
Neurotoxic shellfish posons include at least nine brevctoxins and are
produced by the dinoflagellate Gymnodinium breve. These toxins are
sodium-channel activators, causing repetitive depolarization of nerve
membranes by increasing the sodium ion influx and increasing the frequency of end-plate potentials, ultimately resulting in depletion of neurotransmitted acetylcholine at synapses. In fish and marine mammals
death results most frequently from respiratory failure. Brevetoxins are
heat and cold stable, highly lipid soluble, and presumed to alter the
lipid bilaycr of synaptosomes (Baden and Trainer 1993).
Ciguatoxin
Na+ channel activator
Ciguatera fish poisoning is produced by the dinoflagellates Gambierdiscus toxicus, Ostreops,‘s siamensis, and Prorocentrum lima. Ciguatoxin
is at least a hundred times more potent than brevetoxins and maitoxin
is one of the most potent marine toxins known. Ciguatera toxins arc
highly lipid soluble and mimic the effects of brevetoxins, causing repetitive synaptic stimulation.
Saxitoxin
Na+ channel blocker
Paralytic shellfish poisons include at least a dozen saxitoxins, neosaxitoxins, and gonyautoxins They are produced mainly by members of the
dinoflagellate genera Uexandrium, Gonyaulax, Protogonyaulax, Pyrodinium, and Gymnodinium. These toxins are heat and cold stable, and
water soluble. They are sodium-ion channel blockers that progressively
inhibit nerve conductisln in a dose-dependent manner, relaxing smooth
muscle and causing paralysis and eventually respiratory failure in humans.
Domoic acid
Neuronal depolarization
Amnesic shellfish poisoning is caused by the water-soluble amino acid
domoic acid (DA) produced by some species of diatoms of the genus
Pseudo-nitzschia. The insecticidal activity of DA is apparently due to
its ability to act as a surrogate for the excitatory neurotransmitter
L-glutamic acid. Inability to regulate this substitute transmitter, which
remains attached to the receptor site, causes extensive destructive neuronal depolarization. Similar action of DA on the vertebrate central
nervous system, particularly the hippocampus which contains abundant
glutamate receptors ha:; been proposed by Debonnel et al. (1989).
Thus, amnesic shellfish poisoning is likely due to degeneration of the
hippocampus of the brain.
Diarrhetic shellfish poisons
Enzyme inhibition
Diarrhetic shellfish poisons (see Yasumoto 1990) include okadaic acid
and several other lipid-soluble toxins, and are produced by some species of the dinoflagellae genera Dinophysis and Prorocentrum. These
toxins inhibit protein phosphatase and act directly on specific enzyme
subunits, affecting regulatory processes such as metabolism, membrane
transport secretion, and cell division.
Pjesteria
Neurotoxicity
There is an uncharacterized toxin produced by the dinoflagellate Pjesteria piscicida that produces mortality in fish (Burkholder ct al. 1992)
and neurotoxic symptoms in humans (Glasgow et al. 1995). The mode
of action of this toxin is not known, but exposure to high levels has
resulted in human nervous system dysfunction, elevated hepatic enzyme levels, high phosphorus excretion, and immune system suppression. This toxin seems IO have only minimal effects, if any, on the copepod Acartia tonsa or the rotifer Brachionus plicatilis (Mallin et al.
1995).
toxin
due to poisoning of grazers by phycotoxins,
but it may also
be due to low abundances of grazers or other factors.
We review interactions between toxic phytoplankters and their
grazers, and the accumulation and transport of phycotoxins
through pelagic food webs. Most work has focused on grazing
of metazoans such as copepods feeding on toxic dinoflagellates
and other flagellates, but there is increasing information on interactions between toxic phytoplankters and microzooplanktonic
protists and rotifers, as well as grazing and food-web interactions
with other toxic nonflagellate phytoplankters.
Interactions of toxic phytoplankters with copepods
and other metazooplankton grazers
Dinoflagellate::
seem adversely
and microjlugellates-Some
affected
by toxic dinoflagellates.
copepods
Effects in-
Toxic algae and grazers
elude reduced feeding, egg production, and survival (Gill
and Harris 1987) or avoidance of dinoflagellate-rich layers
during blooms (Fiedler 1982; Huntley 1982).
A chemical component may cause reduced grazing and
avoidance behavior. When clones of Alexandrium tamarense
that varied in toxicity were fed to the copepods Acartia hudsonica and Pseudocalanus sp., ingestion rates decreased with
increasing levels of cellular toxicity (Ives 1985). Copepods
feeding on more toxic clones were paralyzed. Ives (1985,
1987) suggested that chemically induced suppression of
grazing may be due to behavioral rejection of toxic cells
prior to ingestion or ingestion of toxic cells causing progressive paralysis. Ives concluded that physiological incapacitation rather than behavioral rejection of toxic cells was
most likely.
Huntley et al. (1986) tested 13 species or clones of dinoflagellates for rejection by the copepods Calanus pacijcus
and Paracalanus parvus. Five clones were rejected, including two different clones of A. tamarense and Gymnodinium
breve, Scrippsiella trochoidea, and Protoceratium reticulaturn. P. reticulaturn was repeatedly rejected as food by C.
pacijcus. Starved copepods would not feed on it, and copepods maintained with it ceased reproduction and had high
mortality. Both cells and filtrate from P. reticulaturn cultures
reduced feeding on the normally edible dinoflagellate Gyrodinium resplendens. Direct observations with video cinematography (Sykes and Huntley 1987) revealed that feeding
on P. reticulaturn caused reverse peristalsis (“retching”) and
regurgitation in copepods, and G. breve caused elevated
heart rate and loss of motor control. Huntley et al. (1986)
concluded that a physiological reaction rendered copepods
incapable of further feeding on P. reticulaturn and G. breve,
possibly resulting in diminished growth and reproduction,
eventually causing declines in the abundance of grazers. Because dinoflagellate blooms may last for periods of several
weeks, effects of both relaxed grazing pressure and lower
fecundity may be contributing factors to the perpetuation of
toxic blooms.
Uncertainty exists as to whether grazing-inhibitory chemicals are intracellular or extracellular. Heterosigma carterae
and Gymnodinium nagasakiense apparently have intracellular compounds (Uye and Takamatsu 1990), but in P. reticulatum compounds seem to be extracellular (Huntley et al.
1986). Van Alstyne (1986) found that feeding by the copepod Centropages hamatus was suppressed by both intra- and
extracellular compounds of H. carterae and intracellular
chemicals of S. trochoidea. Uye and Takamatsu (1990) concluded that the effects of copepod-flagellate grazing interactions are species-specific.
Two recent studies of copepod grazing on unialgal diets
of toxic Alexandrium isolates gave somewhat different results. Turriff et al. (1995) examined feeding of Calanus finmarchicus adult females from the St. Lawrence estuary on
toxic and nontoxic clones of Alexandrium excavatum. Clearance rates on the nontoxic isolate were high, but near zero
for the toxic strains. When presented with mixtures of nontoxic diatoms and toxic dinoflagellates, copepods avoided
ingesting the dinoflagellates. Although feeding on toxic isolates was low, toxins accumulated in the copepods. In a similar study with Acartia tonsa and Eurytemora herdmani from
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the Gulf of Maine feeding on toxic isolates of Alexandrium
fundyense and A. tamarense, Teegarden and Cembella (1996)
found that neither copepod evidenced incapacitation from
toxins, both accumulated toxins, and both grazed toxic and
nontoxic isolates at high rates. Because responses of the two
copepods were different under the same combinations of
food, or varied with different combinations of food, Teegarden and Cembella concluded that copepod grazing responses
to toxic vs. nontoxic phytoplankters are highly specific for
particular combinations of predators and prey and that presence or absence or relative potency of toxins are not always
the major determinants of any selective feeding response.
Toxic dinoflagellates rarely bloom in nature in the absence
of other phytoplankters so differing responses by various
grazers to specific combinations of toxic and nontoxic prey
likely contribute to differing grazing patterns. Turner and
Anderson (1983) found that during spring blooms of A. tamarense in Cape Cod salt ponds, the copepod A. hudsonica
and planktonic larvae of the polychaete Polydora sp. ate the
toxic dinoflagellate. Feeding rates on the toxic dinoflagellate
were low because of low ambient temperatures and ingestion
of more abundant co-occurring tintinnids and the nontoxic
dinoflagellate Heterocapsa triquetra. There were no apparent adverse effects of ingesting A. tamarense on either copepods or polychaete larvae.
During a massive bloom of the dinoflagellate G. breve off
North Carolina in 1987, Turner and Tester (1989) examined
grazing on natural water samples by five co-occurring species of copepods (A. tonsa, Oncaea venusta, Labidocera aestiva, Centropages typicus, and Paracalanus quasimodo). All
five copepods ingested G. breve, but rates were variable and
generally low. Rates of ingestion of G. breve by A. tonsa,
0. venusta, and L. aestiva increased with increasing natural
concentrations of G. breve up to 2X lo4 cells ml-‘, particularly at levels >3 X 1Oj cells ml- I. C. typicus ingested G.
breve in three of six trials at extremely low rates. P. quasimodo, a small copepod (< 1 mm long), possibly had trouble
ingesting the large (>30 p,m wide) G. breve, and ate little.
In two of the natural water samples used as food, the diatom
Skeletonema costatum was abundant; in both cases, ingestion
of G. breve by A. tonsa, C. typicus, and L. aestiva dropped
to near zero while rates of ingestion of S. costatum remained
high. Thus, these copepods ate the toxic dinoflagellate when
presented with essentially nothing else, but given a choice,
did not. Despite this selection against G. breve the copepods
did not seem adversely affected by 18-22-h incubations. Recent experiments with concentrations of 10” cells liter-’ indicate that A. tonsa can accumulate toxins from G. breve,
become lethargic, but recover after being placed in filtered
seawater (Turner and Tester unpubl. data).
Failure of C. typicus to ingest G. breve during the 1987
North Carolina bloom suggested the possibility of a biogeographic explanation because C. typicus and G. breve rarely
co-occur in nature. G. breve normally blooms in the Gulf of
Mexico and occasionally in the Atlantic off southeastern
Florida. Its presence off North Carolina was due to transport
by the Gulf Stream >lO” km outside its normal range. The
presence of C. typicus south of Cape Hatteras was also adventitious. This copepod is a regular inhabitant of the cooler
waters of the mid-Atlantic and New England continental
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Turner and Tester
shelves (Turner 198 1) and occurs south of Cape Hatteras
only from late autumn through early spring after northeast
winds push Virginia coastal water southwestward (Bowman
1971). Because transport of G. breve via the Gulf Stream
from the Gulf of Mexico to North Carolina coastal waters
was an unprecedented anomalous hydrographic event (Tester
et al. 1989, 1991), both the copepod and the dinoflagellate
co-occurred in waters regularly inhabited by neither. C. typicus possibly did not eat G. breve because it lacked coevolutionary experience counteracting toxins of this dinoflagellate. Conversely, the other copepod species that did eat the
toxic dinoflagellate regularly coexist with G. breve in coastal
waters of the Gulf of Mexico.
If such a biogeographic scenario is valid it may have several important implications. First, it suggests caution in interpreting results of feeding experiments where toxic phytoplankters from a particular location are fed to grazers from
another (Huntley et al. 1986; Ives 1987). Further, because
ballast-water transport inoculates new areas with invading
species of both dinoflagellates (Hallegraeff 1993) and copepods (Carlton and Geller 1993), there is a possibility that
introduction of exotic dinoflagellates or copepods could result in unprecedented encounters favoring bloom development.
Toxic dinoflagellates also can have deleterious effects on
copepod developmental stages. Huntley et al. (1987a) found
that several species of dinoflagellates, including P. reticuZatum and G. breve, were inadequate as food for developing
nauplii of C. pacificus. Nauplii feeding only upon these species developed at rates similar to starved ones and did not
molt past the first feeding stage (N3). G. breve caused nauplii to lose neuromuscular control, become lethargic, and die.
Bagoien et al. (1996) also reported strongly reduced naupliar
activity of Euterpina acutifrons after exposure to Alexandrium minutum and Gymnodinium catenatum. By inhibiting
development of copepod nauplii, toxic dinoflagellates may
enhance their own survival by suppression of future generations of their predators.
There are several studies of copepod grazing on toxic microflagellates, including the raphidophyceans Chattonella
antiqua and H. carterae and the prymnesiophycean microflagellate Chrysochromulina polylepis. Uye (1986) examined
feeding of nine Japanese copepod species on the flagellate
C. antiqua. Three copepod species, thought to be primarily
carnivorous, did not ingest C. antiqua and died within several days. The herbivorous copepods fed on the flagellate
with no adverse effect.
Uye and Takamatsu (1990) investigated feeding by the
copepods Pseudodiaptomus marinus and Acartia omorii on
red tide dinoflagellates, raphidophytes, prasinophytes, and
euglenophytes. Some dinoflagellates, prasinophytes, and euglenophytes were “good quality” food for both copepods,
but other dinoflagellates were good food for one but not the
other. G. nagasakiense and all rhapidophytes were “poor
quality” food for both copepods. These were rejected and
high mortality and low egg production rates resulted. Uye
and Takamatsu determined that ingestion of the edible dinoflagellate H. triquetra was inhibited by filtrate from cell
homogenates of rejected algae, indicating that intracellular
inhibitory chemicals were responsible.
There are contradictory results from different copepod
feeding studies on the same or different flagellates. For instance, H. canerae seemed to be suitable food for A. omorii
(Uye and Tak.amatsu 1990) and C. pacijicus (Sykes and
Huntley 1987), but not for A. hudsonica and A. tonsa (Tomas
and Deason 1981) or C. hamatus (Van Alstyne 1986). P.
reticulaturn was rejected by C. pacificus (Huntley et al.
1986) but not by A. omorii or P. marinus (Uye and Takamatsu 1990).
The microflagellate C. polylepis caused a large toxic
bloom in Scandinavian waters in May 1988 (Rosenberg et
al. 1988; Dahl et al. 1989; Graneli et al. 1989; Maestrini and
Graneli 1991). Nielsen et al. (1990) found that copepods
avoided the dense populations of C. polylepis at the pycnocline and copepod egg production rates from this layer
were lower than for those from above it. In the laboratory,
lower clearance, ingestion, and egg production rates resulted
from A. tonsa feeding on C. polylepis when compared to
feeding on the same concentrations of a similarly sized nontoxic microflagellate Rhodomonas baltica.
Other toxic phytoplankters-Copepod
grazing on nonflagellated toxic phytoplankters include studies with cyanobacteria of the genus Trichodesmium, domoic acid-producing
diatoms of the genus Pseudo-nitzschia, brown tide picoplankters such as Aureococcus anophageflerens, the Texas
brown tide organism, and intermittently gelatinous and possibly oxic prymnesiophytes of the genus Phaeocystis.
Filamentous cyanobacteria commonly produce nuisance
blooms in freshwater and brackish environments (Paerl
1988) and some produce toxins. Filamentous cyanobacteria
of the genus Trichodesmium are a major component of the
marine phytoplankton in tropical and subtropical oceans
(Carpenter 1983). Although some marine harpacticoid copepods feed on Trichodesmium thiebautii (O’Neil and Roman 1992; Sellner 1992), it is toxic to some Calanoid and
cyclopoid copepods, brine shrimp, and mice (Hawser et al.
1992). Other cy anobacteria blooms (Nodularia spumigena)
have been associated with mortality of dogs which came in
contact with affected water (Edler et al. 1985).
Guo and Test’zr (1994) investigated toxicity of Trichodesmium to the copepod A. tonsa during a natural bloom off
North Carolina jn 1992. They found that healthy intact cells
were not toxic to the copepods and were ingested when no
other food was available. Conversely, homogenized cells
were lethal to the copepods, suggesting the presence of intracellular or cell-wall-bound toxins (Falconer 1993). Guo
and Tester (199~:) concluded that effects on grazers may depend on age and physiological state of cells in blooms. Even
for copepods which ingested healthy Trichodesmium cells,
egg production was reduced, suggesting nutritional inadequacy or inefficient assimilation.
Sellner et al. (1994) also found that cyanobacteria were
inadequate food for some zooplankters during cyanobacteria
blooms in the northern Baltic (Gulf of Finland). The copepods Acartia b$losa and Eurytemora afinis fed on the cyanobacterium N. spumigena at rates so low that the copepods
were starving, and A. bijilosa had high mortality and generally appeared ilnhealthy. In contrast, the cladoceran Bosmina longispina maritima seemed to ingest large amounts
Toxic algae and grazers
of cyanobacteria, as indicated by cyanobacteria-associated
pigments in its guts. This was further supported by rapid
movement of cladocerans from cyanobacterial colony to colony, suggesting preferential feeding during the bloom,
In November-December 1987 there was an unprecedented
episode of human shellfish poisoning due to consumption of
mussels (Mytilus edulis) from Prince Edward Island (P.E.I.),
Canada. This resulted in three human deaths and 107 cases
of gastrointestinal illness and amnesic shellfish poisoning
(ASP), or permanent short-term memory loss (Per1 et al.
1990; Todd 1993). The agent for the ASP was the neurotoxin, domoic acid (DA), produced by the diatom Pseudonitzschia multiseries (Bates et al. 1989) which had been ingested by the mussels. This was the first report of shellfish
toxicity due to a diatom. Subsequently there have been
DA-producing blooms at PE.1. in 1988 (Smith et al. 1990)
and in other locations around North America (Villac et al.
1993). Among these was an outbreak of DA toxicity in Monterey Bay, California, where anchovies, having fed on a
bloom of Pseudo-nitzschia australis, were vectors for lethal
seabird intoxication (Fritz et al. 1992; Work et al. 1993). DA
from undigested cells in the anchovy guts points to a short
food chain between the source of the toxin and fish-eating
birds. However, the most likely pelagic consumers of diatoms such as Pseudo-nitzschia would be zooplankters such
as copepods.
Windust (1992) examined the potential of DA to inhibit
grazing by copepods and for copepods to transport DA to
higher trophic levels. Although dissolved DA had dose-dependcnt toxicity for the copepods Temora Zongicornis and
Pseudocalanus acuspes at concentrations in the mg ml-’
range, these concentrations were over three orders of magnitude higher than maximum DA levels measured during the
1988 PE.1. bloom. There was no toxic effect at similar high
levels on the larger copepod Calanus glacialis. To test
whether ingested DA had more profound effects than exposure to dissolved DA, Windust performed several experiments comparing feeding responses of copepods to toxic P.
multiseries and nontoxic P. pungens. There were no differences in feeding rates of C. glacialis and T. Zongicornis on
toxic and nontoxic forms and no apparent effects of DA on
copepod gut-filling rates, feeding behavior, or survival. Copepods were capable of both uptake and retention of ingested
DA because DA was detected after gut evacuation. This finding suggests that copepods may act as mechanisms for vectorial transport of DA to zooplanktivorous consumers, although no cases of higher trophic level impacts have been
reported.
In summers 1985 and 1986 there were unprecedented
blooms of a previously undescribed picoplanktonic (2-3
pm) chrysophyte A. anophageflerens (Sieburth et al. 1988)
at several locations along the northeastern coast of the US,
(Cosper et al. 1989; Smayda and Villareal 1989a). The 1985
brown tide in Narragansett Bay had deleterious effects on
zooplankton and other organisms at several trophic levels
(see Smayda and Fofonoff 1989; Smayda and Villareal
1989b). Included were reduced abundances of the dominant
metazoan zooplankters such as the copepod A. tonsa, depression of the normal summer marine cladoceran community (Evadne nordmani and Podon spp.) to mean abundances
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lo-75-fold lower than in comparison years and fewer eggs
of the anchovy Anchoa mitchilli (10% of nonbrown tide
years). When the brown tide in Narragansett Bay was minimal and short-lived in summer 1986, some of these inimical
effects reversed and there were more cladocerans and bay
anchovy eggs.
There were similar ecosystem disruptions during Long Island brown tides in 1985 and 1986 (Cosper et al. 1987).
Although most of the zooplankton of Great South Bay on
the south shore of Long Island did not exhibit reduced abundances during the 1985 bloom compared to the reduced 1986
bloom, abundances of summer bivalve larvae were an order
of magnitude higher in 1986 than in 1985 (Duguay et al.
1989). This suggests that bay scallop recruitment failures in
1985 (Bricelj et al. 1987) may have been due to starvation
of planktonic larvae (Gallagher et al. 1989).
There are several indications that the brown tide blooms
were largely ungrazed by metazoans. Durbin and Durbin
(I 989) found that when the copepod A. tonsa collected from
brown tide water were fed the palatable diatom Thalassiosira
weissflogii they had higher feeding and egg production rates
than on a diet of brown tide algae. These measurements indicated that copepods were severely food limited in Narragansett Bay during the brown tide and starvation may have
been the major cause of plankton decreases during the 1985
blooms.
Since 1990 a brown tide has also frequented portions of
the south Texas coast (Buskey and Stockwell 1993; Stockwell et al. 1993; Whitledge 1993). As noted for the northeastern U.S. brown tides, there have also been substantial
declines in populations of mesozooplankton, dominated by
the copepod A. tonsa (Buskey and Stockwell 1993). Reductions in A. tonsa body size, gut pigment content, and egg
production during the brown tide suggest that this alga was
poorly grazed. The cause of the unpalatability of brown tide
algae is not clear, but Tracey et al. (1988) suggested that an
external layer of polysaccharidelike material covering the
cell may interfere with motion of mussel gill cilia, either by
clogging or chemical irritants or toxicants.
Phaeocystis is an important bloom-forming genus in temperate and polar seas (Davidson and Marchant 1992). The
life cycle of Phaeocystis includes solitary flagellated cells
3-8 p,rn in diameter, as well as colonial aggregations of hundreds of nonflagellated cells embedded in gelatinous matrices of up to 2-mm diameter (Rousseau et al. 1994).
Gelatinous Phaeocystis colonies can form enormous nuisance blooms contributing to anoxia, beach fouling, and
clogging of bivalve gills and fishing nets (Lancelot et al.
1987, WeiBe et al. 1994). Phaeocystis may also be toxic in
that the antibiotic acrylic acid (Sieburth 1960) or dimethylsulfide (Liss et al. 1994) may be either contained in or excreted from colonies,
The gelatinous and(or) possibly toxic nature of this alga
has led to what Huntley et al. (1987b) called the “legend of
Phaeocystis unpalatibility to zooplankton” (see Tande and
Bamstedt 1987; WeiBe et al. 1994). This possibility is supported by numerous observations of reduced abundances of
zooplankton associated with Phaeocystis blooms (Davies et
al. 1992; Turner 1994). There are numerous indications from
field and laboratory studies that blooms of colonial Phaeo-
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Turner and Tester
cystis are not extensively grazed by or are even deleterious
to copepods (Schnack et al. 1985; Verity and Smayda 1989).
During a spring bloom in the English Channel, Bautista et
al. (1992) found that there were lower levels of copepod gut
fluorescence, ingestion rates, and copepod abundance during
a period of Phaeocystis abundance than during a previous
period of diatom dominance. Combining individual copepod
ingestion rates with copepod abundances allowed Bautista et
al. to conclude that community grazing impact was minimal
during the bloom, mainly due to anomalously low copepod
abundances (Davies et al. I992).
Reduced grazing on Phaeocystis could also be due to poor
nutritional value. During a bloom in the Irish Sea, Phaeocystis had a low content of polyunsaturated fatty acids and
vitamin C; comparison of the biochemical composition of
copepod fecal pellets and Phaeocystis revealed that copepods fed primarily on diatoms rather than Phaeocystis during
the bloom (Claustre et al. 1990).
interactions of toxic phytoplankters with
microzooplanktonic grazers
Protists-Interactions
between toxic phytoplankton and
microzooplankton have been less-studied than those with copepods and results are mixed. Although some tintinnids selectively prey upon toxic and nontoxic dinoflagellates, other
dinoflagellates are poor food (Stoecker et al. 1981). Exudates
of A. tamarense and Alexandrium ostenfeldii cause reversals
of ciliary motion in some tintinnids with abnormal continuous backwards swimming or death (Hansen 1989; Hansen
et al. 1992). Also several tintinnid species exhibit reduced
growth and survival on diets of toxic dinoflagellates such as
Gyrodinium aureolum (Hansen 1995) or other toxic Aagellates that are not dinoflagellates such as H. carterae and C.
polylepis (Verity and Stoecker 1982; Carlsson et al. 1990).
Heterotrophic dinoflagellate species may consume other
toxic bloom-formers. Several laboratory studies suggest that
predation of heterotrophic dinoflagellates on autotrophic dinoflagellates could be an important regulator of red tide
bloom development and decline (Jeong and Latz 1994; Nakamura et al. 1992, 1995; Burkholder and Glasgow 1995).
Also some tintinnids and heterotrophic dinoflagellates can
ingest free-swimming solitary Phaeocystis cells or pick solitary cells off of gelatinous colonies (Admiraal and Venekamp 1986; WciBe and Scheffel-M&er 1990).
Rotifers-Solne
toxic algae are ingested by rotifers with
varying effects. Mallin et al. (1995) found that feeding on
the toxic dinoflagellate Pfiesteria piscicida caused no apparent deleterious effects in terms of reduced fecundity or increased mortality on the rotifer Brachionus plicatilis, but this
rotifer exhibited reduced feeding compared to nontoxic algae
on H. carterae (Chotiyaputta and Hirayama 1978) and Texas
brown tide (Buskey and Hyatt 1995). H. carterae was also
not ingested by the marine rotifer Synchaeta Cecilia (Egloff
3986) and this alga inhibited feeding on other acceptable
phytoplankters at abundances as low as 50 cells ml- I and
reduced rotifer survival and reproduction at levels > 10X I Oj
cells ml- I. Egloff (1988) found that S. Cecilia did not eat
toxic A. tamarense, as well as numerous other phytoplankton
and diatom species known to be nontoxic. Thus, rotifers like
other grazers, exhibit varied responses when feeding on various toxic phytoplankters and results of such interactions are
highly specific for particular combinations of predators and
prey *
Accumulation, transport, and effects of phycotoxins
in pelagic food webs
Grazers function as vectors for transport of phycotoxins
to zooplanktor, predators such as fish. Most information on
this subject comes from the seminal work on paralytic shellfish poisoning (PSP) toxins from A. tamarense in the Bay
of Fundy (Whl te 1977, 1979, 1980, 1981a).
During a fish kill accompanying an A. tamarense bloom
in July, 1976, stomachs of dead adult Atlantic herring (Clupea harengus narengus) contained algal remains, pteropods
(Limacina retroversa), and PSP toxins. Comparable levels
of PSP toxins ..n adult herring resulted in immediate abnormal swimming behavior, paralysis within tens of minutes,
and death withj n 2 h. White (I 977) concluded that PSP toxins had been ingested by eating pteropods which had grazed
on A. tamaren&e.
During a blos3m in 1977, PSP toxins were found in plankton samples obtained with net meshes of 20, 64, 243, and
571 pm. Maximum toxin content was in the >20-pm fraction, dominated by A. tamarense; progressively lower toxin
levels were found in net fractions dominated by tintinnids
with ingested A. tamarense (>64 pm), marine cladocerans,
and small copepods (>243 km) and larger copepods (>57 I
km). Because there were no dinoflagellates or tintinnids in
the larger net fractions, White (1979) concluded that these
larger zooplankters had accumulated toxins through ingestion. Levels of PSP toxin in these larger fractions were higher than those shown to be lethal to small adult herring, suggesting that dense blooms of A. tamarense could cause
substantial mortality of fish by ingestion of PSP-containing
zooplankton.
In subsequenl kills of adult herring during A. tamarense
blooms, dying fish were observed swimming abnormally and
gulping for breal:h, and stomachs of dead fish contained algal
residue, PSP toxins, and were packed with marine cladocerans (E. nordmani) which also contained A. tamarense remains. Zooplankton samples dominated by E. nordmani also
contained toxins. PSP toxins were present only in fish viscera and were absent from muscle tissue, indicating that toxins ingested through zooplankton vectors quickly kill fish.
White (1980) concluded that there was strong circumstantial
evidence that fish kills during toxic algal blooms were from
fish eating intoxified zooplankton such as the pteropods in
the 1976 bloom or the cladocerans during the 1979 bloom.
He noted that in a 1968 sand lance kill during a Gonyaulax
bloom in British waters (Adams et al. 1968), that E. nordmani had also bl:en a dominant zooplankter, and ingestion
of toxin-contaminated zooplankton had also been suggested
(but not demonstrated) to be the cause of the fish kill.
White (1981a,r used laboratory experiments to confirm
that A. hudsoniw and barnacle nauplii could ingest toxic A.
Toxic algae and grazers
tamarense and accumulate toxins with no apparent adverse
effects. Toxins were retained in the organisms for several
days after gut evacuation, suggesting incorporation into somatic tissues. Turriff et al. (1995) and Teegarden and Cembella (1996) subsequently confirmed that Alexandrium spp.
toxins accumulate in several other species of copepods (C.
jinmarchicus, A. tonsa, E. herdmani) and Boyer et al. (1985)
found that Protogonyaulax catenella toxin accumulates in
the copepod Tigriopus californicus.
Additional studies have confirmed that dinoflagellate toxins are lethal to larvae, juveniles, or adults of several species
of fish. Intoxication can be by direct exposure to toxin, ingestion of toxic dinoflagellates, or ingestion of zooplankton
that had ingested dinoflagellates (White 1981b; White et al.
1989; Mills and Klein-Macphee 1979; Gosselin et al. 1989;
Huntley 1989; Riley et al. 1989; Robineau et al. 19916; Nielsen 1993).
Robineau et al. (199lb) compared feeding by larvae of
the Atlantic mackerel (Scomber scorn&us) and the lobster
(Homarus americanus) on toxic A. excavatum, and adult copepods that had eaten toxic A. excavatum. Lobster larvae
were apparently unaffected, but poisoned fish larvae exhibited the same symptoms of erratic swimming, sinking, and
immobility prior to death recorded for other studies. These
results, combined with those from cited studies on fish, adult
crabs, crab larvae, bivalves, euphausiids, copepods, and lobsters led Robineau et al. (199 la) to suggest that invertebrates
can generally accumulate PSP toxins without lethal effects,
whereas nervous systems of fish, humans, and other vertebrates are far more susceptible to lethal inhibition of axonal
conduction by sodium channel blocking.
First-feeding larvae of various fish species ingest dinoflagellates or herbivorous zooplankton (Turner 1984), so
phycotoxins could potentially cause significant mortality on
emerging year-classes of fish if their critical period for larval
feeding and survival (Hjort 1914; Lasker 1971) coincided
with blooms of toxic dinoflagellates. Many later stage larvae
and postlarvae, although primarily zooplanktivorous and less
susceptible to direct intoxication, still might be at risk of
vectorial intoxication.
Impact of zooplankton grazing on development and
persistence of harmful algal blooms
Impacts of zooplankton community grazing pressure on
development and termination of toxic phytoplankton blooms
arc variable and outcomes appear situation-specific. During
spring blooms of A. tamarense in Cape Cod embayments in
1980, Turner and Anderson (1983) measured rates of rcmoval of A. tamarense by copepods and planktonic polychaete larvae from mixtures of natural seawater spiked with
A. tamarense cultures. Because of low individual grazing
rates due to cold temperatures and low abundances of copepods, copcpod community grazing impact on A. tamarense
populations was minimal, with a maximum removal of only
1% d -I. This was not the case, however, for polychaete larvae because they were very abundant (855 liter- I). Even
with lower individual grazing rates than copepods it was
estimated that the population of polychaete larvae could re-
1209
move > 100% of the A. tamarense population daily. Populations of A. tamarense and polychaete larvae crashed within
days of each other, the latter crash likely caused by larval
settlement. Whether such a process translocates toxins from
the plankton to the benthos is unknown. During the same
blooms, Watras et al. (1985) measured both dinoflagellate
growth rates and zooplankton community grazing rates with
radioactive tracers and concluded that loss of A. tamarense
to grazers could play a significant role in regulating timing
and magnitude of blooms in these embayments because
community grazing rates often exceeded rates of dinoflagellate population growth.
Uye (1986) estimated copepod community grazing impact
on development of C. antiqua blooms in the Seto Inland Sea
of Japan. At minimum field concentrations (20 cells ml-l),
copepod communities could daily graze 3.4-30.8% of the
C. antiqua population. Grazing pressure decreased with increasing C. anfiqua abundance, with only 1.8% of the C.
antiqua population removed at maximum field abundance
levels. Uye concluded that copepod grazing pressure could
be important in retarding the initial stages of bloom development when both water temperature and concentrations of
C. antiqua were low. However, under conditions favorable
for flagellate growth, copepod grazing pressure would be
vastly exceeded by C. antiqua growth, so that at peak abundance levels (>500 cells ml-‘), the bloom would be virtually
immune to grazing impact.
Sellner and Olson (1985) also found minimal losses to
copepod grazing during dinoflagellate blooms in Chesapeake
Bay and its embayments-generally
<5% of field dinoflagellate populations per day for E. afinis grazing on H. triquetra, and A. tonsa feeding on Katodinium rotundatum and
Gymnodinium nelsoni. Sellner et al. (199 1) found that daily
grazing impact by rotifers, copepods, and copepod nauplii
on a winter bloom of K. rotundatum in the Patuxent River
estuary of Chesapeake Bay increased from 13% of dinoflagellate biomass in December to 67% during the peak bloom
and copepod abundance period in February. Sellner et al.
(199 1) concluded that grazing could remove substantial portions of this bloom, contributing to its demise in early
March. This situation was atypical of other Chesapeake Bay
dinoflagellate blooms where grazing imposed only minimal
losses (Sellner and Brownlee 1990).
There is considerable evidence that the northeastern U.S.
and Texas brown tide blooms may have been triggered by
breakdowns in grazing at several trophic levels. Although
picoplankters the size of A. anophag&erens can be eaten by
filter-feeding bivalves (Tracey 1988), most grazing on these
small cells would be presumed from heterotrophic protists.
Mesozooplanktonic suspension-feeders such as copepods are
thought to be unable to efficiently graze on picoplankters,
but copepods are known to prey on the heterotrophic protists
that eat picoplankters (Turner and Roff 1993). Thus, the relative levels of predation by copepods on heterotrophic protists, and of these protists on brown tide picoplankters, may
be important factors in bloom development.
Caron et al. (1989) examined consumption of brown tide
organisms by planktonic protists and estimated the effects of
this picoplankter on microprotistan grazing in Long Island
embayments. Brown tide algae supported rapid growth of
1210
Turner and Tester
some heterotrophic protists but allowed only slow growth or
no growth of others. Addition of A. anophagefirens to natural water promoted increases in abundance of protists and
decreases in the brown tide alga, suggesting grazing by protists. Estimates of predation on fluorescently labeled algae
or bacteria by natural assemblages of protists in Long Island
waters affected by brown tide revealed no reduction of protistan grazing during brown tide blooms. Together these observations suggest that protistan grazing should keep levels
of brown tide algae reduced to the point of retarding bloom
development but that a critical factor may be the abundance
of potential protistan consumers of brown tide algae at the
time of bloom initiation, because once a bloom becomes
established, it appears capable of explosively outgrowing
protistan predation. Caron et al. speculated that heavy predation by larger zooplankters on the protistan predators of
brown tide algae may provide ephemeral windows of opportunity for successful initiation of brown tide blooms.
Smayda and Villareal (1989b) concluded that the 1985
brown tide in Narragansett Bay may also have been triggered
during a period of reduced grazing. They proposed that during the late spring-early summer transition from winterspring bloom to summer conditions there is an open niche
in the phytoplankton of Narragansett Bay and that competition for and occupancy of this niche can be determined by
complex trophic interactions. In some cases the toxic flagellate H. carterae wins the competition by allelochemic inhibition of the frequently dominant, rapidly growing diatom
S. costatum (Pratt 1966). In other cases, S. costatum blooms
in summer because ctenophore predation on copepods reduces copepod grazing pressure on diatoms (Deason and
Smayda 1982) or H. carterae blooms because its toxicity
inhibits copepod grazing (Tomas and Deason 1981).
Smayda and Villareal (19896) suggested that the 1985 and
1986 brown tides may have been differentially regulated by
heterotrophic flagellate grazing. During the latter half of
summer 1985 abundance of brown tide algae declined while
phagotrophic flagellate abundance increased. The implication is that the flagellates grazed down the brown tide until
its disappearance in October 1985. Brown tide reappeared in
high abundance (up to 254X 10” cells liter-‘) in mid-May
1986, persisting through June when it co-occurred with a
bloom of H. carterae and minimal levels of S. costatum.
This was the reverse of the 1985 situation when S. costatum
was abundant and H. carterae was not. However, the most
substantial difference in early summer 1986 was high abundance of heterotrophic
gymnodiniacean
dinoflagellates
which presumably prevented the brown tide algae from developing further, unlike the previous year when the dinoflagellates had not been abundant. Jn essence, A. anophagefferens won the competition
for the open niche in
Narragansett Bay in 1985 but was prevented from doing so
by heterotrophic flagellates in 1986. Once the 1985 bloom
developed after initial failure of heterotrophic flagellate predation, the brown tide itself reduced the impact of grazing
by metazoan zooplankton (copepods and cladocerans), exacerbating a third grazing collapse by bivalves. Smayda and
Villareal (1989b) suggested that failures in grazing may be
more common contributors
to harmful phytoplankton
blooms than is generally realized. Reductions in microzoo-
plankton abundance and grazing rates before and after brown
tide development support the conclusion that the Texas
brown tide bloom was largely uncontrolled by grazing (Buskey and Stockwell 1993).
Conclusions
An overall synthesis of interactions between toxic phytoplankton and their grazers is elusive because blooms and
grazer interactions are situation-specific. Many contradictions are due to a variety of toxins which may have different
physiological effects on consumers and to differences in toxin potency or intracellular concentrations due to genetic variability, uncontrolled culture conditions, or environmental
variations that are not accounted for in natural blooms. Different grazers also exhibit different responses to different
toxic phytoplankton species or to different clones or blooms
of the same spl=cies. Additional complications can arise from
effects of organisms at other trophic levels that, while not
direct grazers of toxic phytoplankton, may affect their
blooms by preying on their grazers. Accordingly, information from one experimental study or natural bloom is difficult to extrapolate to another.
Despite this complexity, it is clear that improved understanding of to.uic phytoplankton blooms will emerge with
more effort to define the role of zooplankton grazers. Both
zooplankton population monitoring and studies of zooplankton grazing and food-web interactions should be incorporated into phytoplankton monitoring programs focused on
harmful blooms. In the very few cases where ongoing phytoplankton and zooplankton monitoring preceded development of a harmful bloom (e.g. Buskey and Stockwell 1993;
Buskey and Hyatt 1995), the impact of zooplankton grazing,
or its absence, seemed important in bloom dynamics.
We recommend that studies of toxic phytoplankton, grazers, and food-web interactions be conducted with more attention to variations in intracellular toxin concentrations and
potency. Also, grazing studies should extend beyond unialgal cultures to include ingestion of naturally co-occurring
nontoxic as well as toxic phytoplankters in natural assemblages. Through collaboration between phytoplanktologists,
zooplanktologists, and phycotoxin chemists a better understanding of interactions between toxic phytoplankton, their
grazers, and marine food webs will emerge.
References
ABBOTT, B., AND A. WHIT)J. 1979. Toxigenesis in dinoflagellates,
p. 494-496. In Toxic dinoflagellate blooms: Proc. 2nd Int.
Conf. Elsevicr.
ADAMS, J. A., D. D, SEATON, J. B. BUCHANAN, AND M. R. LONGBOTTOM. 19138.Biological observations associated with the
toxic phytoplankton bloom off the east coast. Nature 220: 2425.
W., AND L. A. H. VHNEKAMP. 1986. Significance of
tintinnid grazing during blooms of Phaeocystis pouch&ii (Haptophyccae) in Dutch coastal waters. Neth. J. Sea Res. 20: 61-
ADMIKAAI,,
66.
1992. Marine biotoxins at
the top of the food chain. Oceanus 35(3): 55-6 1.
ANDEKSON, D. M., AND A. W. WIIITE.
-,
D. M. KLILIS, G. J. DOUCE’TTE, J. C. GALLAGHER, AND E.
Toxic algae and grazers
1994. Biogeography of toxic dinoflagellates in the
genus Alexandrium from the northeastern United States and
Canada. Mar. Biol. 120: 467-478.
J. J. SUJ,LIVAN, S. HAJ.L, ANU C. Lnn. 1990. Dynamics and physiology of saxitoxin production by the dinoflagellates Alexundrium spp. Mar. Biol. 104: 5 1l-524.
BALIEN, D. G., T, J. MENIX, AND R. E. BIXXK. 1979. Two similar
toxins isolated from Gymnodinium breve, p. 327-334. In Toxic
dinoflagellate blooms: Proc. 2nd Int. Conf. Elsevier.
AND C. R. TOMAS. 1988. Variations in major toxin composition for six clones of Ptychodiscus brevis. Toxicon 26:
961-963.
-,
AND B. L. TRAINER. 1993. Mode of action of toxins of
seafood poisoning, p. 49-47. Zn I. R. Falconer [ed.], Algal
toxins in seafood and drinking water. Academic.
BAG@JEN, E., A. MIRANDA, B. R~CXJERA, AND J. M. FRANCO. 1996.
Effects of two paralytic shellfish toxin producing dinoflagellates on the pelagic harpacticoid copepod Euterpina acutifrons.
Mar. Biol. 126: 361-369.
BATES, S. S., AND OT~IELIS. 1989. Pennate diatom Nitzschia pungens as the primary source of domoic acid, a toxin in shellfish
from eastern Prince Edward Island, Canada. Can. J. Fish.
Aquat. Sci. 46: 1203-1215.
AND OTJJERS. 1991, Controls on domoic acid production
by’the diatom Nitzschia pungens f. multiseries in culture: Nutrients and irradiance. Can. J. Fish. Aquat. Sci. 48: 1136-l 144.
-,
J, WORMS, AND J. C. SMJTJI 1993. Effects of ammonium
and nitrate on growth and domoic acid production by Nitzschia
pungens in batch culture. Can. J. Fish. Aquat. Sci. 50: 12481254.
BAU~JSTA, B., R. l? HARRIS, I? R. C. TRANTER, AND D. HARBOUK.
1992. In situ copepod feeding and grazing rates during a spring
bloom dominated by Phueocystis sp. in the English Channel.
J. Plankton Res. 14: 69 l-703.
BOWMAN, T. E. 197 1. The distribution of Calanoid copepods off
the southeastern United States between Cape Hatteras and
southern Florida. Smithson. Contrib. Zool. 96: l-58.
BOYEK, G. L., J. J. SULUVAN, M. LEBLANC, AND R. J. ANDERSEN.
1985. The assimilation of PSP toxins by the copepod Tigriopus culifornicus from dietary Protogonyuulux catenellu, p.
407-412. Zn Toxic dinoflagellates: Proc. 3rd Int. Conf. Elsevier.
BRJCELJ, V. M., J. EPP, AND R. E. MALOUF. 1987. Intraspecific
variation in reproductive and somatic growth cycles of bay
scallops Argopecten irradiuns. Mar. Ecol. Prog. Ser. 36: 123137.
BUIIKJIOLDER, J. M., AND H. B. GLASGOW, JR. 1995. Interactions
of a toxic estuarine dinoflagellate with microbial predators and
prey. Arch. Protistenkd. 145: 177-188.
-,
AND C. W. HOBHS. 1995. Fish kills linked to a
toxic ambush-predator dinoflagellate: Distribution and environmental considerations. Mar. Ecol. Prog. Ser. 124: 43-61.
-,
E. J. NOGA, C. W. HOBBS, H. B. GJ.AXOW, JR., AND S. A.
SMJTM. 1992. New “phantom” dinoflagellate is the causative
agent of major estuarine fish kills. Nature 358: 407-410.
BUSKEY, E. J., AND C. J. HYA’I’T. 1995. Effects of the Texas (USA)
“brown tide” alga on planktonic grazers. Mar. Ecol. Prog. Ser.
124: 285-292.
AND D. A. SIXXKWIXL.
1993. Effects of a persistent
“blown tide” on zooplankton populations in the Laguna Madre
of south Texas, p. 659-666. Zn Toxic phytoplankton blooms in
the sea. Proc. 5th Int. Conf. on Toxic marine phytoplankton.
Elsevier.
CARLSSON, I?, E. GJIANBLI, AND I? OLSSON. 1990. Grazer elimination through poisoning: One of the mechanisms behind
Chrysochromulinu polylepis blooms?, p. 116-l 22. In Toxic
marine phytoplankton: Proc. 4th Int. Conf. Elsevier.
BALKIJ.
1211
CARLTON, J. T,, AND J. B. GEI.LER. 1993. Ecological roulette: The
global transport of nonindigenous marine organisms. Science
261: 78-82.
CARON, D. A., E. L. LJM, H. K~NZE, E. M. COSP~~R, AND D. M.
ANDERSON. 1989. Trophic interactions between nano- microzooplankton and the “brown tide,” p. 265-294. In E. M. Cosper et al. [eds.], Novel phytoplankton blooms. Causes and impacts of recurrent brown tides and other unusual blooms.
Springer.
CARPEN’TER, E. J. 1983. Physiology and ecology of marine planktonic Oscillatoriu (Trichodesmium). Mar. Biol. Lett. 4: 69-85.
CEMBELJ,A, A. D., AND J. C. TEJERRJAULT. 1989. Population dynamics and toxin composition of Protogonyaulux tamurensis
from the St. Lawrence estuary, p, 81-84. Zn Red tides. Biology,
environmental science, and toxicology. Proc. 1st Int. Symp. on
Red Tides. Elscvicr.
AND P BEI~AND. 1988. Toxicity of cultured isolates and natural populations of Protogonyaulux tamarensis
from the St. Lawrence estuary. J. Shellfish Res. 7: 611-621.
CHOTIYAPUI’TA, C., AND K. HIKAYA~VIA. 1978. Food selectivity of
the rotifer Brachionus plicutilis feeding on phytoplankton. Mar.
Biol. 45: 105-l 11.
CI,AUSTRD, H., ANJI OT’MERS. 1990. A biochemical investigation of
a Phueocystis sp. bloom in the Irish Sea. J. Mar. Biol. Assoc.
U.K. 70: 197-207.
COSPER, E. M., V. M. BRICEIJ, AND E. J. CARPENTER [IDS.]. 1989.
Novel phytoplankton blooms. Causes and impacts of recurrent
brown tides and other unusual blooms. Springer.
AND OTIJERS. 1987. Recurrent and persistent brown tide
blooms perturb coastal marine ecosystem. Estuaries 10: 284290.
DAIJL, E., 0. LINDAHL, E. PAASCHE, AND J. TJ-~R~NIX~~N. 1989. The
Chrysochromulinu polylepis bloom in Scandinavian waters
during spring 1988, p. 383-405. Zn E. M. Cosper et al. [eds.],
Novel phytoplankton blooms. Causes and impacts of recurrent
brown tides and other unusual blooms. Springer.
DALE, B., AND C. M. YENTSCM. 1978. Red tide and paralytic shellfish poisoning. Oceanus 21(3): 41-49.
DAVIDSON, A. T., AND H. J. MAJKHANT.
1992. The biology and
ecology of Phaeocystis (Prymnesiophyceae). Prog. Phycol.
Rcs. 8: l-45.
DAVIES, A. G., AND OTHERS. 1992. The ecology of a coastal Phaeocystis bloom in the north-western English Channel in 1990. J.
Mar. Biol. Assoc. U.K. 72: 691-708.
DEASON, E. E., AND T. J. SMAYDA. 1982. Ctenophore-zooplanktonphytoplankton interactions in Narragansett Bay, Rhode Island,
during 1972-1977. J. Plankton Res. 4: 203-217.
DEBONNEL, G., L. BEAUCHESNE, ANL) C. J>EMONTIC~NY. 1989. Domoic acid the alleged “mussel toxin,” might produce its neurotoxic effect through kainate receptor activation: An electrophysiological study in the rat dorsal hippocampus. Can. J.
Physiol. Pharmacol. 67: 29-33.
DOUCE’J‘TB, G. J. 1995. Interactions between bacteria and harmful
algae: A review. Nat. Toxins 3: 65-74.
DUGUAY, L. E., D. M. MON’I’ELEONI!, AND C.-E. QUAGLJE’ITA. 1989.
Abundance and distribution of zooplankton and ichthyoplankton in Great South Bay, New York during the brown tide outbreaks of 1985 and 1986, p. 599-623. In E. M. Cosper et al.
[eds.l, Novel phytoplankton blooms. Causes and impacts of
recurrent brown tides and other unusual blooms. Springer.
DURBJN, A. G., AND E. G. DURBJN. 1989. Effect of the “brown
tide” on feeding, size and egg laying rate of adult female Acurtin tonsa, p. 625-646. In E. M. Cosper et al. [edsl, Novel
phytoplankton blooms. Causes and impacts of recurrent brown
tides and other unusual blooms. Springer.
EDLER, L., S. FIZRN~, M. G, LJND, R. LUNDRERG, AND F? 0. NJLS-
1212
Turner and Tester
SON. 1985. Mortality of dogs associated with a bloom of the
cyanobacterium Nod&aria spumigena in the Baltic Sea. Ophelia 24: 103-109.
EC~LOE‘F,
D. A. 1986. Effects of Olisthodiscus Zuteus on the feeding
and reproduction of the marine rotifer Synchaetu Cecilia. J.
Plankton Res. 8: 263-274.
-.
1988. Food and growth relations of the marine microzooplankter, Synchaeta Cecilia (Rotifera). Hydrobiologia
157:
129-141.
FALCONER, I. R. 1993. Measurement of toxins from blue-green
algae in water and foodstuffs, p. 165-175. In I. R. Falconer
[ed.], Algal toxins in seafood and drinking water. Academic.
FIEDL,ER, F! C. 1982. Zooplankton avoidance and reduced grazing
responses to Gymnodinium splendens (Dinophyceae). Limnol.
Oceanogr. 27: 96 I -965.
FLYNN, K. J., AND K. FJ,YNN. 1995. Dinoflagellate physiology: Nutrient stress and toxicity, p. 541-550. In Harmful marine algal
blooms, Proc. 6th Int. Conf. on Toxic Marine Phytoplankton.
Lavoisier.
FREEBERG, L. R., A. MARSHAJ,L, AND M. HEYL. 1979. Interrelationships of Gymnodinium breve (Florida red tide) within the
phytoplankton community, p. 139-144. Zn Toxic dinoflagellate
blooms: Proc. 2nd Int. Conf. Elsevier.
FRITZ, L., M. A. QUILLJAM, J. L. C. WRIGHT, A. M. BBALE, AND
T. M. WORK. 1992. An outbreak of domoic acid poisoning
attributed to the pennate diatom Pseudonitzschia uustrulis. J.
Phycol. 28: 439-442.
GALLAGHER, S. M., D. K. STOFXXER, AND V. M. BRJCBLJ. 1989.
Effects of the brown tide alga on growth, feeding physiology
and locomotory behavior of scallop larvae (Argopecten irrudiuns), p. 5 1l-541. Zn E. M. Cosper et al. [eds.], Novel phytoplankton blooms. Causes and impacts of recurrent brown
tides and other unusual blooms. Springer.
GERACJ, J. R., AND OTHERS. 1989. Humpback whales (Megupteru
novueangliue) fatally poisoned by dinoflagellate toxin. Can. J.
Fish. Aquat. Sci. 46: 1895-1898.
GIJ,J,, C. W. AND R. I? HARRIS. 1987. Behavioural responses of the
copepods Culunus helgolundicus and Temoru longicornis to
dinoflagellate diets, J. Mar. Biol. Assoc. U.K. 67: 785-801.
GJ,ASGOW, H. B., JR., J. M. BURKHOLDER, D. E. SCI-JMECHEL, F? A.
TESTEIZ, AND F! A. RUBLEIX. 1995. Insidious effects of a toxic
estuarine dinoflagellate on fish survival and human health. J.
Toxicol. Environ. Health 46: 501-522.
GOSSELJN, S., L. FORTIER, AND J. A. GAGNB. 1989. Vulnerability
of marine fish larvae to the toxic dinoflagellate Protogonyuulux
tamarensis. Mar. Ecol. Prog. Ser. 57: l-10.
GRANI~LJ, E., AND O’TJ-JDRS. 1989. From anoxia to fish poisoning:
The last ten years of phytoplankton blooms in Swedish marinc
waters, p. 407-427. In E. M. Cosper et al. [eds.], Novel phytoplankton blooms. Causes and impacts of recurrent brown
tides and other unusual blooms. Springer.
~
B. SUNDSTROM, L. EDLER, AND D. M. ANDERSON [EDS.].
1990. Toxic marine phytoplankton: Proc. 4th Int. Conf. Elsevicr.
Guo, C., AND P A. TESTER. 1994. Toxic effect of the bloom-forming Trichodesmium sp. (Cyanophyta) to the copepod Acartia
tonsa. Nat. Toxins 2: 222-227.
HALLEGRAGFF, G. M. 1993. A review of harmful algal blooms and
their apparent global increase. Phycologia 32: 79-99.
HANSEN, I? J. 1989. The red tide dinoflagellate Alexundrium tumarense: Effects on behaviour and growth of a tintinnid ciliate.
Mar. Ecol. Prog. Ser. 53: 105-l 16.
-,
1995. Growth and grazing response of a ciliate feeding on
the red tide dinoflagellate Gyrodinium aureolum in monoculture and in mixture with a non-toxic alga. Mar. Ecol. Prog. Ser.
121: 65-72.
-,
A. D. CEMB~~J,LA, AND 0. MOESTRUP. 1992. The marine
dinoflagellate Alexundrium ostenfeldii: Paralytic shellfish toxin
concentration, composition, and toxicity to a tintinnid ciliate.
J. Phycol. 28: 597-603.
HAWSEJI, S. I?. J. M. O’NEJJ,, M. R. ROMAN, AND G. A. CODD.
1992. Toxicity of blooms of the cyanobacterium Trichodesmium to zooplankton. J. Appl. Phycol. 4: 79-86.
HAY, M. E. 1991. Marine-terrestrial
contrasts in the ecology of
plant cherrical defenses against herbivores. Trends Ecol. Evol.
6: 362-365.
HJORT, J. 1914. Fluctuations in the great fisheries of northern Europe viewed in the light of biological research. Rapp. P-V.
Reun. Cons. Perm. Int. Explor. Mer 20. 228 p.
HUNTLEY, M. El. 1982. Yellow water in La Jolla Bay, California,
July 1980. 2, Suppression of zooplankton grazing. J. Exp. Mar.
Biol. Ecol. 63: 81-91.
-.
1989. Larval feeding of northern anchovy, Engruulis mordux, on dinoflagellates: Implications for year class strength.
Sci. Mar. 53: 239-245.
l? CJMJNJEJ,LO, AND M. D. G. LOPEZ. 1987~. Importance
of ‘food quality in determining development and survival of
Cu/anus paci$cus (Copepoda: Calanoida). Mar. Biol. 95: 103113.
I? SYKIIS, S. ROHAN, AND V. MARJN. 1986. Chemicallymediated rejection of dinoflagellate prey by the copepods Culanus pacijrus and Parucalanus purvus: Mechanism, occurrence and significance. Mar. Ecol. Prog. Ser. 28: 105-120.
K. TANDE, AND H. C. EJLERTSEN. 19876. On the trophic
fate of Phucocystis pouchetii (Hariot). 2. Grazing rates of Calanus hyperboreus (Kroyer) on diatoms and different size categories of Phueocystis pouchetii. J. Exp. Mar. Biol. Ecol. 110:
197-212.
IVES, J. D. 1985. The relationship between Gonyaulux tumarensis
cell toxin levels and copepod ingestion rates, p. 423-4 18. In
Toxic dinoflagellates: Proc. 3rd Int. Conf. Elsevicr.
-.
1987. .Possible mechanisms underlying copepod grazing
responses to levels of toxicity in red tide dinoflagellates. J.
Exp. Mar. Eiol. Ecol. 112: 131-145.
JEONG, H. J., AND M. I. LATZ. 1994. Growth and grazing rates of
the heterotrophic dinoflagellates Protoperidinium spp. on red
tide dinoflagellates. Mar. Ecol. Prog. Ser. 106: 173-185.
KIM, Y. S., AND D. E MARTIN. 1974. Effects of salinity on synthesis of DNA, acidic polysaccharide, and ichthyotoxin in
Gymnodinium breve. Phytochemistry 13: 533-538.
KODAMA, M. 1990. Possible links between bacteria and toxin production in algal blooms, p, 52-6 1. Zn Toxic marine phytoplankton: Proc. 4th Int. Conf. Elscvier.
LANCELOT, C., A VD OTHERS. 1987. Phueocystis blooms and nutrient enrichment in the continental coastal zones of the North
Sea. Ambio 16: 38-46.
LASKER, R. 1971. Field criteria for survival of anchovy larvae: The
relation between inshore chlorophyll maximum layers and successful first leeding. Fish. Bull. 73: 453-462.
LASSUS, l?, G. AFXJJ,, E. ERARD, F? GENTIEN, AND C. MARCAJLJX~IJ
[EDS.]. 1995. Harmful marine algal blooms. Proc. 6th Int.
Conf. on Toxic Marine Phytoplankton. Lavoisicr.
LJSS, F? S., G. M/,J,JN, S. M. TURNER, AND F? M. HOLI,JGAN. 1994.
Dimethyl sulphide and Phueocystis: A review. J. Mar. Syst. 5:
41-53.
MAESTRINI, S. Y., AND E. GRAN~I.J. 1991. Environmental conditions and eccaphysiological mechanisms which led to the 1988
Chrysochromulina polylepis bloom: An hypothesis. Oceanol.
Acta 14: 397-413.
MAJ,LJN, M. M., J. M. BURKHOLDER, L. M. LARSEN, AND H. B.
GLAX;OW, Jh. 1995. Response of two zooplankton grazers to
an ichthyotoxic estuarine dinoflagellate. J. Plankton Res. 17:
35-363.
Toxic algae and grazers
L., D. M. ANDERSON, ANII Y. SHIMUXJ. 1985. Comparison of toxicity between populations of GonyauZux tamnrensis
of eastern North American waters. Estuarine Coastal Shelf Sci.
21: 401-410.
MILIS, L. J., AND G. KLEIN-MACPHEE.
1979. Toxicity of the New
England red tide dinoflagellate to winter flounder larvae, p.
389-394. In Toxic dinoflagellate blooms: Proc. 2nd Int. Conf.
Elsevier.
NAKAMURA, Y., S.-Y. SUZUKI, AND J. HIROMI. 1995. Growth and
grazing of a naked heterotrophic dinoflagellate, Gyrodinium
dominans. Aquat. Microb. Ecol. 9: 157-164.
Y. YAMAZAKI, AND J. HIROMI. 1992. Growth and grazing
of ‘a heterotrophic dinoflagellate, Gyrodinium dominans, fccding on a red tide flagellate, ChattoneZZa antiqun. Mar. Ecol.
Prog. Ser. 82: 275-279.
NIELXN, M. V. 1993. Toxic effect of the marinc dinoflagellate
Gymnodinium galatheanum on juvenile cod Gadus morhua.
Mar. Ecol. Prog. Ser. 95: 273-277.
NIEI..SEN, T. G., T. KI@RBOE, AND l? K. BJ~RNSEN. 1990. Effects of
a Chrysochromulina polylepis subsurface bloom on the planktonic community. Mar. Ecol. Prog. Ser. 62: 21-35.
O’NEIL, J. M., AND M. R. ROMAN. 1992. Grazers and associated
organisms of Trichodesmium, p. 61-73. Zn E. J. Carpenter
[ed.], Marinc pelagic cyanobacteria: Trichodesmium and other
diazotrophs. Kluwer.
PAEIIL, H. W. 1988. Nuisance phytoplankton blooms in coastal,
estuarine, and inland waters. Limnol. Oceanogr. 33: 823-847.
PHRI,, T. M., AND OTHERS. 1990. An outbreak of toxic enccphalopathy caused by eating mussels contaminated with domoic acid.
N. Eng. J. Med. 322: 1775-1780.
PRATT%, D. M. 1966. Competition between Skeletonema costutum
and Olisthodiscus Zuteus in Narragansett Bay and in culture.
Limnol. Oceanogr. 11: 447-455.
RIIEY, C. M., S. A. HOLT, G. J. HOLT, E. J. BUSKEY, AND C. R.
ARNOI~D. 1989. Mortality of larval red drum (Sciaenops ocelZatus) associated with a Ptychodiscus brevis red tide. Contrib.
Mar. Sci. 31: 137-146.
ROBINEAU, B., L. FORTIRR, J. A. GAC;NI?, AND A. D. CEMBELI.A.
1991a. Comparison of the response of five larval fish species
to the toxic dinotlagellatc Alexandrium excavatum (Braarud)
Balcch. J. Exp. Mar. Biol. Ecol. 152: 225-242.
---,
J. A. GAGNI?, L. FORTIER, AND A. D. CEMBELI.A. 1991b.
Potential impact of a toxic dinoflagellate (Alexandrium excavatum) bloom on survival of fish and crustacean larvae. Mar.
Biol. 108: 293-301.
ROSENBEII<;, R., 0. LINDAHL,, AND H. BUNCK.
1988. Silent spring
in the sea. Ambio 17: 289-290.
ROUSSEAU, V., AND OTIIERS. 1994. The lift cycle of Phaeocystis
(Prymnesiophyceac): Evidence and hypotheses. J. Mar. Syst.
5: 23-39.
SCIINACK, S. B., V. SMBTACEK, B. VON BODUNGHN, AND I? STEGMANN. 1985. Utilization of phytoplankton by copepods in antarctic waters during spring, p. 65-81. In J. S. Gray and M. E.
Christiansen [eds.], Marine biology of polar regions and effects
of stress on marinc organisms. Wiley.
SCUNEII, K. G. 1992. Trophodynamics of marine cyanobacteria
blooms, p. 75-94. In E. J. Carpenter [cd.], Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Kluwer.
AND D. C. BROWNLEE. 1990. Dinoflagellate-microzooplankton interactions in Chesapeake Bay, p. 221-226. In Toxic
marine phytoplankton: Proc. 4th Int. Conf. Elsevier.
-,
R, V. LACOU’I’UKE, S. J. CIBIK, A. BRINDLEY, AND S. G.
BROWNI,EI!. 199 1. Tmportancc of a winter dinoflagellate-microflagellate bloom in the Patuxent River estuary. Estuarine
Coastal Shelf Sci. 32: 27-42.
9 AND M. M. OL,SON. 1985. Copepod grazing in red tides
MARANDA,
1213
of Chcsapcake Bay, p. 245-250. Zn Toxic dinoflagellates: Proc.
2nd Int. Conf. Elsevier.
AND K. KONONHN. 1994. Copcpod grazing in a
summer cyanobacteria bloom in the Gulf of Finland. Hydrobiologia 292/293: 249-254.
S~~UMWAY, S. E. 1990. A review of the cffccts of algal blooms on
shellfish and aquaculture. J. World Aquaculture Sot. 21: 65105.
-,
AND T. L. Cuccr.
1987. The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behavior
of the bivalve molluscs. Aquat. Toxicol. 10: 9-27.
SIHBURTII, J. McN. 1960. Acrylic acid, an “antibiotic”
principle
in Phaeocystis blooms in antarctic waters. Science 132: 676_ 677.
-,
F! W. JOI~NSO&I, AND I? E. HAI<(;RAVGS. 1988. Ultrastructure and ecology of Aureococcus anophageflerens Gcn. et sp.
nov. (Chrysophyceae); the dominant picoplankter during a
bloom in Narragansett Bay, Rhode Island, summer 1985. J.
Phycol. 24: 4 16-425.
SMAYDA, T J. 1989. Primary production and the global epidemic
of phytoplankton blooms in the sea: a linkage?, p. 449-483.
In E. M. Cosper et al. [eds.], Novel phytoplankton blooms.
Causes and impacts of recurrent brown tides and other unusual
blooms. Springer.
ANr) P FOF;ONOFF. 1989. An extraordinary, noxious browntide in Narragansett Bay. 2. Inimical effects, p. 133-136. In
Red tides. Biology, environmental science, and toxicology.
Proc. 1st Int. Symp. on Red Tides. Elscvier.
AND Y. S~IIMIZU [EIX.]. 1993. Toxic phytoplankton blooms
in ;he sea. Proc. 5th Int. Conf. on Toxic Marinc Phytoplankton.
Elsevicr.
-,
AND T A. VIILARBAI..
1989~. An extraordinary, noxious
brown-tide in Narragansett Bay. 1. The organism and its dynamics, p. 129-132. Zn Red tides: Biology, environmental science, and toxicology. Proc. 1st Int. Symp. on Red Tides. Elscvier.
-,
AND -.
1989b. The 1985 “brown-tide” and the open
phytoplankton niche in Narragansett Bay during summer, p.
159-187. In E. M. Cosper et al. [cds.], Novel phytoplankton
blooms. Causes and impacts of recurrent brown tides and other
unusual blooms. Springer,
SMITII, J. C., AND OTHEIIS. 1990. Toxic blooms of the domoic acid
containing diatom Nitzschia pungens in the Cardigan River,
Prince Edward Island, in 1988, p. 227-232. In Toxic marine
phytoplankton: Proc. 4th Int. Conf. Elsevier.
STEIDINGER, K. A. 1983. A rc-evaluation of toxic dinoflagellate
biology and ecology. Prog. Phycol. Res. 2: 147-188.
STOCKWI’U, D. A., E. J. BUSKEY, AND T E. WHITIEIXE.
1993.
Studies on conditions conducive to the development and maintenance of a persistent “brown tide” in Laguna Madre, Texas,
p. 693-698. Zn Toxic phytoplankton blooms in the sea. Proc.
5th Int. Conf. on Toxic Marine Phytoplankton. Elscvier.
STOECKHR, D. K., R. R. L. GUILI~ARD, AND R. M. KAVEIJ. 1981.
Selective predation by Favella ehrenbergii (Tintinnia) on and
among dinoflagellates. Biol. Bull. 160: 136-145.
SYKES, P. E, AND M. E. HUNTLEY. 1987. Acute physiological reactions of Calanus pacificus to selected dinoflagellates: Direct
observations. Mar. Biol. 94: 19-24.
TANDE, K. S., AND U. BAMSTED’~. 1987. On the trophic fate of
Phaeocystis pouchetii (Hariot). I. Copepod feeding rates on
solitary cells and colonies of P. pouchetii. Sarsia 72: 3 13-320.
TAYI,~R, E J. R. 1990. Red tides, brown tides and other harmful
algal blooms: The view into the 1990’s, p. 527-533. Zn Toxic
marinc phytoplankton: Proc. 4th Int. Conf. Elsevier.
TEEGARDEN, G. J., AND A. D. CEMBELI,A. 1996. Grazing of toxic
dinoflagellates, Alexandrium spp., by adult copepods of coastal
1214
Turner and Tester
P/Taine: Implications for the fate of paralytic shellfish toxins in
marine food webs. J. Exp. Mar. Biol. Ecol. 196: 145-176.
TESTI%, l? A., l? K. FOWLER, AND J. T, TURNER. 1989. Gulf Stream
transport of the toxic red tide dinoflagellate, Ptychodiscus brevis, from Florida to North Carolina, p. 349-358. Zn E. M. Cosper et al. [eds.], Novel phytoplankton blooms, Causes and impacts of recurrent brown tides and other unusual blooms,
Springer.
-,
R. I? STUMPF, E M. VUKOVICH, P K. FOWLER, AND J. T..
TURNER. 1991. An expatriate red tide: Transport, distribution,
and persistence. Limnol. Oceanogr. 36: 1053-1061.
TODD, E. C. D. 1993. Domoic acid and amnesic shellfish poisoning-a review. J. Food Protect. 56: 69-83.
TOMAS, C. R., AND E. E. DBASON. 1981. The influence of grazing
by two Acartia species on Olisthodiscus Zuteus Carter. Mar.
Ecol. 2: 215-223.
TRACEY, G. A. 1988. Feeding reduction, reproductive failure, and
mortality in Mytilus edulis during the 1985 “brown tide” in
Narragansett Bay, Rhode Island. Mar. Ecol. Prog. Ser. 50: 7381.
-,
l? W. JOHNSON, R. W. STEELE, I? E. HARGRAVES, AND J.
McN. SIERURTM. 1988. A shift in photosynthetic picoplankton
composition and its effect on bivalve mollusc nutrition: The
1985 “brown tide” in Narragansett Bay, Rhode Island. J.
Shellfish Res. 7: 671-675.
TURNER, J. T. 198 1. Latitudinal patterns of Calanoid and cyclopoid
copepod diversity in estuarine waters of eastern North America. J. Biogeogr. 8: 369-382.
-.
1984. The feeding ecology of some zooplankters that are
important prey items of larval fish. NOAA Tech. Rep. NMFS
7. 28 p.
1994. Planktonic copepods of Boston Harbor, Massachuse& Bay and Cape Cod Bay, 1992. Hydrobiologia 292/293:
405-413.
AND D. M. ANDERSON. 1983. Zooplankton grazing during
di;oflagellate blooms in a Cape Cod embayment, with observations of predation upon tintinnids by copepods. Mar. Ecol.
4: 359-374.
AND J. C. ROFF. 1993. Trophic levels and trophospecies
in karine plankton: Lessons from the microbial food web. Mar.
Microb. Food Webs 7: 225-248.
AND I? A. TESTER. 1989. Zooplankton feeding ecology:
Cdpepod grazing during an expatriate red tide, p, 359-374. In
E. M. Cosper et al. [eds.], Novel phytoplankton blooms. Causes and impacts of recurrent brown tides and other unusual
blooms. Springer.
TURRIFF, N., J. A. RUNGE, AND A. D. CEMBELLA. 1995. Toxin
accumulation and feeding behaviour of the planktonic copepod
Calanus jinmarchicus exposed to the red-tide dinoflagellate AZexandrium excavatum. Mar. Biol. 123: 55-64.
UYE, S. 1986. Impact of copepod grazing on the red-tide flagellate
Chattonella antiqua. Mar. Biol. 92: 35-43.
AND K. TAKAMATSU. 1990. Feeding interactions between
planktonic copepods and red-tide flagellates from Japanese
coastal waters. Mar. Ecol. Prog. Ser. 59: 97-107.
VAN ALSTYNE, K. L. 1986. Effects of phytoplankton taste and
smell on feeding behavior of the copepod Centropages hamatus. Mar. Ecol. Prog. Ser. 34: 187-190.
VERITY, I? G., AND T, J. SMAYDA. 1989. Nutritional value of
Phneocystis pouchetii (Prymnesiophyceae) and other phyto-
plankton for Acartia spp. (Copepoda): Ingestion, egg production, and growth of nauplii. Mar. Biol. 100: 161-171.
-,
AND D. STOECKER. 1982. Effects of Olisthodiscus Zuteus
on the growth and abundance of tintinnids. Mar. Biol. 72: 7987.
VILLAC, M. C., D. L. ROELKE, T. A. VILLAREAL., AND G. A. FRYXELL. 1993. Comparison of two domoic acid-producing diatoms: A re view. Hydrobiologia 269/270: 213-224.
WATRAS, C. J., V. C. GARCON, R. J. OLSON, S. W. CMSHOLM, AND
D. M. ANDERSON. 1985. The effect of zooplankton grazing on
estuarine blooms of the toxic dinoflagellate Gonyaulux tamarensis. J. Plankton Res. 7: 891-908.
WEIOE, T., AND U. ScHEFF&-M<jSER. 1990. Growth and grazing
loss in single-celled Phaeocystis sp. (Prymnesiophyceae). Mar.
Biol. 106: 153-158.
-,
K. TANDE, I? VERITY, E HANSEN, AND W. GIESKES. 1994.
The trophic significance of Phaeocystis blooms. J. Mar. Syst.
5: 67-79.
WHITE, A. W. 1977. Dinoflagellate toxins as probable cause of an
Atlantic helring (Clupea harengus hnrengus) kill, and pteropods as apparent vector. J. Fish. Res. Bd. Can. 34: 2421-2424.
-.
1979. Dinoflagellate toxins in phytoplankton and zooplankton frictions during a bloom of Gonyaulax excavatu, p.
381-384. In Toxic dinoflagellate blooms: Proc. 2nd Int. Conf.
Elsevier.
-.
1980. Recurrence of kills of Atlantic helTing (Clupea harengus harengus) caused by dinoflagellate toxins transferred
through herbivorous zooplankton. Can. J. Fish. Aquat. Sci. 37:
2262-2265.
-.
198 la. Marine zooplankton can accumulate and retain dinoflagellate toxins and cause fish kills. Limnol. Oceanogr. 26:
103-109.
-.
1981b. Sensitivity of marine fishes to toxins from the redtide dinoflagellate Gonyaulax excavatu and implications for
fish kills. M.ir. Biol. 65: 255-260.
0. FUKLHARA, AND M. ANRAKU. 1989. Mortality of fish
larbae from eating toxic dinoflagellates or zooplankton containing dinoflagellate toxins, p. 395-398. In Red tides: Biology,
environment;11 science, and toxicology. Proc. 1st Int. Symp. on
Red Tides. Elsevier.
WHITLEDCX, T. E 1993. The nutrient and hydrographic conditions
prevailing in Laguna Madre, Texas before and during a brown
tide bloom, p, 71 l-71 6. Zn Toxic phytoplankton blooms in the
sea. Proc. 5t.l Int. Conf. on Toxic Marine Phytoplankton. Elsevier.
WINDUST, A. 1992. The responses of bacteria, microalgae and
zooplankton to the diatom Nitzschia pungens f. multiseries
and its toxic metabolite domoic acid. M.S. thesis, Dalhousie
Univ. 107 p.
-,
J. L. C. ‘WRIGHT, AND J. L. MCLACHLAN.
1996. The effccts of the diarrhetic shellfish poisoning toxins, okadaic acid
and dinophysistoxin-1, on the growth of microalgae. Mar. Biol.
126: 19-25.
WORK, T. M., AI\D OTHERS. 1993. Domoic acid intoxication of
brown pelicans and cormorants in Santa Cruz, California, p.
643-649. Zn Toxic phytoplankton blooms in the sea. Proc. 5th
Int. Conf. on Toxic Marine Phytoplankton. Elsevier.
YASUMOTO, T. 19!)0. Marinc microorganisms toxins-an overview,
p. 3-8. Zn Tclxic marine phytoplankton: Proc. 4th Int. Conf.
Elsevier.
YENTSCH, C. M. 1981. Flow cytometric analysis of cellular saxitoxin in the dinoflagellate Gonyaualx tamarensis var. excavatu.
Toxicon 19: 6 11-62 1.